Atomic structure of clathrin: A β propeller terminal domain joins an α zigzag linker

Cell

Volumn 95, Issue 4, 1998, Pages 563-573

  Ter Haar, Ernst ^a   Musacchio, Andrea ^c   Harrison, Stephen C ^b,c   Kirchhausen, Tomas ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN;

ARTICLE; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

TRISKELION;

EID: 0032514995     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81623-2     Document Type: Article

References (75)

1. Boll, W., Ohno, H., Songyang, Z., Rapoport, I., Cantley, L.C., Bonifacino, J.S., and Kirchhausen, T. (1996). Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 15, 5789-5795.
2. Brünger, A.T. (1992). X-PLOR Version 3.1:A System for X-Ray Crystallography and NMR. (New Haven, Connecticut: Yale University Press).
3. Carson, M. (1991). Ribbons 2.0. J. Appl. Crystallogr. 24, 958-961.
4. Clairmont, K.B., Boll, W., Ericsson, M., and Kirchhausen, T. (1997). A role for the hinge/ear domain of the beta chains in the incorporation of AP complexes into clathrin-coated pits and coated vesicles. Cell. Mol. Life Sci. 53, 611-619.
5. Collaborative Computational Project, Number 4. (1994). The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr. D 50, 760-763.
6. Conti, E., Uy, M., Leighton, L, Blobel, G., and Kuriyan, J. (1998). Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin α. Cell 94, 193-204.
7. Crowther, R.A., and Pearse, B.M. (1981). Assembly and packing of clathrin into coats. J. Cell Biol. 91, 790-797.
8. Csukai, M., Chen, C.H., Dematteis, M.A., and Mochlyrosen, D. (1997). The coatomer protein beta′-COP, a selective binding protein (RACK) for protein kinase cepsilon. J. Biol. Chem. 272, 29200-29206.
9. Das, A.K., Cohen, P.W., and Barford, D. (1998). The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17, 1192-1199.
10. Dasso, M., Seki, T., Azuma, Y., Ohba, T., and Nishimoto, T. (1994). A mutant form of the Ran/TC4 protein disrupts nuclear function in Xenopus laevis egg extracts by inhibiting the RCC1 protein, a regulator of chromosome condensation. EMBO J. 13, 5732-5744.
11. Dawson, T.M., Arriza, J.L., Jaworsky, D.E., Borisy, F.F., Attramadal, H., Lefkowitz, R.J., and Ronnett, G.V. (1993). Beta-adrenergic receptor kinase-2 and beta-arrestin-2 as mediators of odorant-induced desensitization. Science 259, 825-829.
12. Diviani, D., Lattion, A.L., Larbi, N., Kunapuli, P., Pronin, A., Benovic, J.L., and Cotecchia, S. (1996). Effect of different G protein-coupled receptor kinases on phosphorylation and desensitization of the alpha(1b)-adrenergic receptor. J. Biol. Chem. 277, 5049-5058.
13. Evans, S.V. (1993). SETOR: hardware lighted three-dimensional solid model representation of macromolecules. J. Mol. Graph. 11, 134-138.
14. Freedman, N.J., Liggett, S.B., Drachman, D.E., Pei, G., Caron, M.G., and Lefkowitz, R.J. (1995). Phosphorylation and desensitization of the human beta(1)-adrenergic receptor - involvement of G protein-coupled receptor kinases and CAMP-dependent protein kinase. J. Biol. Chem. 270, 17953-17961.
15. Gallusser, A., and Kirchhausen, T. (1993). The β1 and β2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J. 12, 5237-5244.
16. Glickman, J.N., Conibear, E., and Pearse, B.M.F. (1989). Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin-like growth factor II receptor. EMBO J. 8, 1041-1047.
17. Goodman, O.B., Jr., Krupnick, J.G., Santini, F., Gurevich, V.V., Penn, R.B., Gagnon, A.W., Keen, J.H., and Benovic, J.L. (1996). β-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature 383, 447-450.
18. Goodman, O.B., Jr., Krupnick, J.G., Gurevich, V.V., Benovic, J.L., and Keen, J.H. (1997). Arrestin/clathrin interaction. Localization of the arrestin binding locus to the clathrin terminal domain. J. Biol. Chem. 272, 15017-15022.
19. Gorina, S., and Pavletich, N.P. (1996). Structure of the P53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2. Science 274, 1001-1005.
20. Granzin, J., Wilden, U., Choe, H.W., Labahn, J., Krafft, B., and Buldt, G. (1998). X-ray crystal structure of arrestin from bovine rod outer segments. Nature 391, 918-921.
21. Heilker, R., Manningkrieg, U., Zuber, J.F., and Spiess, M. (1996). In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO J. 15, 2893-2899.
22. Heuser, J., and Kirchhausen, T. (1985). Deep-etch views of clathrin assemblies. J. Ultrastruct. Res. 92, 1-27.
23. Huang, K.M., Gullberg, L, Nelson, K.K., Stefan, C.J., Blumer, K., and Lemmon, S.K. (1997). Novel functions of clathrin light chains: clathrin heavy chain trimerization is defective in light chain-deficient yeast. J. Cell Sci. 110, 899-910.
24. Huber, A.H., Nelson, W.J., and Weis, W.I. (1997). Three-dimensional structure of the armadillo repeat region of beta-catenin. Cell 90, 871-882.
25. Jones, T.A., Zou, J.-Y., and Cowan, S.W. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119.
26. Keen, J.H., Willingham, M.C., and Pastan, I.H. (1979). Clathrincoated vesicles: isolation, dissociation and factor-dependent reassociation of clathrin baskets. Cell 16, 303-312.
27. Kirchhausen, T., and Harrison, S.C. (1981). Protein organization in clathrin trimers. Cell 23, 755-761.
28. Kirchhausen, T., and Harrison, S.C. (1984). Structural domains of clathrin heavy chains. J. Cell Biol. 99, 1725-1734.
29. Kirchhausen, T., Harrison, S.C., Parham, P., and Brodsky, F.M. (1983). Location and distribution of the light chains in clathrin trimers. Proc. Natl. Acad. Sci. USA 80, 2481-2485.
30. Kirchhausen, T., Harrison, S.C., and Heuser, J. (1986). Configuration of clathrin trimers: evidence from electron microscopy. J. Ultrastruct. Res. 94, 199-208.
31. Kirchhausen, T., Harrison, S.C., Chow, E.P., Mattaliano, R.J., Ramachandran, K.L., Smart, J., and Brosius, J. (1987a). Clathrin heavy chain: molecular cloning and complete primary structure. Proc. Natl. Acad. Sci. USA 84, 8805-8809.
32. Kirchhausen, T., Scarmato, P., Harrison, S.C., Monroe, J.J., Chow, E.P., Mattaliano, R.J., Ramachandran, K.L., Smart, J.E., Ahn, A.H., and Brosius, J. (1987b). Clathrin light chains LCA and LCB are similar, polymorphic and share repeated heptad motifs. Science 236, 320-324.
33. Kirchhausen, T., Bonifacino, J.S., and Riezman, H. (1997). Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9, 488-495.
34. Kleywegt, G. J., and Jones, T.A. (1994). From first map to final model. In Proceedings of the CCP4 Study Weekend, S. Bailey, R. Hubbard, and D. Waller, eds. (Daresbury, UK: Daresbury Laboratory), pp. 59-66.
35. Krupnick, J.G., Goodman, O.B., Jr., Keen, J.H., and Benovic, J.L (1997). Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus. J. Biol. Chem. 272, 15011-15016.
36. Lambright, D.G., Sondek, J., Bohm, A., Skiba, N.P., Hamm, H.E., and Sigler, P.B. (1996). The 2.0 Å crystal structure of a heterotrimeric G protein. Nature 379, 311-319.
37. Lefkowitz, R.J., Inglese, J., Koch, W.J., Pitcher, J., Attramadal, H., and Caron, M.G. (1992). G-protein-coupled receptors: regulatory role of receptor kinases and arrestin proteins. Cold Spring Harbor Symp. Quant. Biol. 57, 127-133.
38. Lemmon, S.K., Pellicena Palle, A., Conley, K., and Freund, C.L. (1991). Sequence of the clathrin heavy chain from Saccharomyces cerevisiae and requirement of the COOH terminus for clathrin function. J. Cell Biol. 112, 65-80.
39. 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.
40. Lohse, M.J., Benovic, J.L., Codina, J., Caron, M.G., and Lefkowitz, R.J. (1990). beta-Arrestin: a protein that regulates beta-adrenergic receptor function. Science 248, 1547-1550.
41. Morris, S.A., Schröder, S., Plessmann, U., Weber, K., and Ungewickell, E. (1993). Clathrin assembly protein AP180: primary structure, domain organization and identification of a clathrin binding site. EMBO J. 12, 667-675.
42. Murphy, J.E., Pleasure, I.T., Puszkin, S., Prasad, K., and Keen, J.H. (1991). Clathrin assembly protein AP-3. The identity of the 155K protein, AP 180, and NP185 and demonstration of a clathrin binding domain. J. Biol. Chem. 266, 4401-4408.
43. Murzin, A.G. (1992). Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 14, 191-201.
44. Näthke, I.S., Heuser, J., Lupas, A., Stock, J., Turck, C.W., and Brodsky, F.M. (1992). Folding and trimerization of clathrin subunits at the triskelion hub. Cell 68, 899-910.
45. 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 clathrinassociated proteins. Science 269, 1872-1875.
46. Otwinowski, Z. (1991). Maximum likelihood refinement of heavy atom parameters. In Isomorphous Replacement and Anomalous Scattering, W. Wolf, P.R. Evans, and A.G.W. Leslie, eds. (Warrington, UK: Science and Engineering Council/Daresbury Laboratory), pp. 80-86.
47. Otwinowski, Z. (1993). Oscillation data reduction program. In Data Collection and Processing, L. Sawyer, N. Isaacs, and S. Bailey, eds. (Warrington, UK: Science and Engineering Research Council/ Daresbury Laboratory), pp. 56-62.
48. Pearse, B.M. (1976). Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl. Acad. Sci. USA 73, 1255-1259.
49. Pearse, B.M.F. (1988). Receptors compete for adaptors found in plasma membrane coated pits. EMBO J. 7, 3331-3336.
50. Pearse, B.M., and Robinson, M.S. (1984). Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J. 3, 1951-1957.
51. Peranen, J., Rikkonen, M., Hyvonen, M., and Kaariainen, L. (1996). T7 vectors with modified T7 lac promoter for expression of proteins in Escherichia coli. Anal. Biochem. 236, 371-373.
52. Pippig, S., Andexinger, S., Daniel, K., Puzicha, M., Caron, M.G., Lefkowitz, R.J., and Lohse, M.J. (1993). Overexpression of beta-arrest in and beta-adrenergic receptor kinase augment desensitization of beta 2-adrenergic receptors. J. Biol. Chem. 268, 3201-3208.
53. Ramjaun, A.R., and McPherson, P.S. (1998). Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J. Neurochem. 70, 2369-2376.
54. Rapoport, I., Miyazaki, M., Boll, W., Duckworth, B., Cantley, LC., Shoelson, S., and Kirchhausen, T. (1997). Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J. 9, 2240-2250.
55. Rapoport, I., Chen, Y.C., Cupers, P., Shoelson, S.E., and Kirch-hausen, 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.
56. Renault, L., Nassar, N., Vetter, I., Becker, J., Klebe, C., Roth, M., and Wittinghofer, A. (1998). The 1.7 Å crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature 392, 97-101.
57. Robinson, M.S. (1994). The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6, 538-544.
58. Saxena, K., Gaitatzes, C., Walsh, M.T., Eck, M., Neer, E.J., and Smith, T.F. (1996). Analysis of the physical properties and molecular modeling of Sec13 - a WD repeat protein involved in vesicular traffic. Biochemistry 35, 15215-15221.
59. Scarmato, P., and Kirchhausen, T. (1990). Analysis of clathrin light chain-heavy chain interactions using truncated mutants of rat liver light chain LCB3. J. Biol. Chem. 265, 3661-3668.
60. Schmid, S.L., Matsumoto, A.K., and Rothman, J.E. (1982). A domain of clathrin that forms coats. Proc. Natl. Acad. Sci. USA 79, 91-95.
61. Shih, W., Gallusser, A., and Kirchhausen, T. (1995). A clathrin-binding site in the hinge of the β-2 chain of mammalian AP-2 complexes. J. Biol. Chem. 270, 31083-31090.
62. 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.
63. Sondek, J., Bohm, A., Lambright, D.G., Hamm, H.E., and Sigler, P.B. (1996). Crystal structure of a G-protein beta gamma dimer at 2.1 Å resolution. Nature 379, 369-374.
64. Sorkin, A., and Carpenter, G. (1993). Interaction of activated EGF receptors with coated pit adaptins. Science 261, 612-615.
65. Sosa, M.A., Schmidt, B., von Figura, K., and Hille-Rehfeld, A. (1993). In vitro binding of plasma membrane-coated vesicle adaptors to the cytoplasmic domain of lysosomal acid phosphatase. J. Biol. Chem. 268, 12537-12543.
66. Springer, T.A. (1998). Extracellular β-propeller module predicted in lipoprotein scavenger receptors, tyrosine kinases, epidermal growth gactor precursor and extracellular matrix components. J. Mol. Biol., in press.
67. Trowbridge, I.S., Collawn, J.F., and Hopkins, C.R. (1993). Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9, 129-161.
68. Ungewickell, E. (1983). Biochemical and immunological studies on clathrin light chains and their binding sites on clathrin triskelions. EMBO J. 8, 1401-1408.
69. Ungewickell, E., and Branton, D. (1981). Assembly units of clathrin coats. Nature 289, 420-422.
70. Ungewickell, E., Unanue, E.R., and Branton, D. (1982). Functional and structural studies on clathrin triskelions and baskets. Cold Spring Harbor Symp. Quant. Biol. 46(2), 723-731.
71. Vigers, G.P., Crowther, R.A., and Pearse, B.M. (1986). Three-dimensional structure of clathrin cages in ice. EMBO J. 5, 529-534.
72. Wall, M.A., Coleman, D.E., Lee, E., Iniguez-Lluhi, J.A., Posner, B.A., Gilman, A.G., and Sprang, S.R. (1995). The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 83, 1047-1058.
73. Wilde, A., and Brodsky, F.M. (1996). In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135, 635-645.
74. Winkler, F.K., and Stanley, K.K. (1983). Clathrin heavy chain, light chain interactions. EMBO J. 2, 1393-1400.
75. Zaremba, S., and Keen, J.H. (1983). Assembly polypeptides from coated vesicles mediate reassembly of unique clathrin coats. J. Cell Biol. 97, 1339-1347.