Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport

Nature Structural Biology

Volumn 10, Issue 5, 2003, Pages 386-393

  Shiba, Tomoo ^a,b   Kawasaki, Masato ^a   Takatsu, Hiroyuki ^c,d   Nogi, Terukazu ^a,e   Matsugaki, Naohiro ^a   Igarashi, Noriyuki ^a   Suzuki, Mamoru ^a   Kato, Ryuichi ^a   Nakayama, Kazuhisa ^c,f   Wakatsuki, Soichi ^a  

^a INSTITUTE OF MATERIALS STRUCTURE SCIENCE   (Japan)

^b Foundation for Advancement of International Science   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d RIKEN YOKOHAMA INSTITUTE   (Japan)

^e MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^f KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ARF PROTEIN; BINDING PROTEIN; CLATHRIN; GGA PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; GOLGI COMPLEX; HUMAN; LYSOSOME; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; CIRCULAR DICHROISM; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; GUANOSINE TRIPHOSPHATE; HUMANS; KINETICS; LYSOSOMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-GOLGI NETWORK;

EID: 0037407395     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb920     Document Type: Article

References (37)

1. Robinson, M.S. & Bonifacino, J.S. Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444-453 (2001).
2. Boman, A.L., Zhang, C.-J., Zhu, X. & Kahn, R.A. A family of ADP-ribosylation factor effectors that can alter membrane transport through the trans-Golgi. Mol. Biol. Cell 11, 1241-1255 (2000).
3. Dell'Angelica, E.C. et al. GGAS: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J. Cell Biol. 149, 81-93 (2000).
4. Hirst, J., Lui, W.W., Bright, N.A., Totty, N., Seaman, M.N. & Robinson, M.S. A family of proteins with γ-adaptin and VHS domains that facilitate trafficking between the trans-Golgi network and the vacuole/lysosome. J. Cell Biol. 149, 67-79 (2000).
5. Poussu, A., Lohi, O. & Lehto, V.-P. Vear, a novel Golgi-associated protein with VHS and γ-adaptin "ear" domains. J. Biol. Chem. 275, 7176-7183 (2000).
6. Takatsu, H., Yoshino, K. & Nakayama, K. Adaptor γ ear homology domain conserved in γ-adaptin and GGA proteins that interact with γ-synergin. Biochem. Biophys. Res. Commun. 271, 719-725 (2000).
7. Nielsen, M.S. et al. The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J. 20, 2180-2190 (2001).
8. Puertollano, R., Aguilar, R.C., Gorshkova, I., Crouch, R.J. & Bonifacino, J.S. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292, 1712-1716 (2001).
9. Zhu, Y., Doray, B., Poussu, A., Lehto, V.-P. & Kornfeld, S. Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science 292, 1716-1718 (2001).
10. Takatsu, H., Katoh, Y., Shiba, Y. & Nakayama, K. Golgi-localizing, γ-adaptin ear homology domain, ADP-ribosylation factor-binding (GGA) proteins interact with acidic dileucine sequences within the cytoplasmic domains of sorting receptors through their Vps27p/Hrs/STAM (VHS) domains. J. Biol. Chem. 276, 28541-28545 (2001).
11. Doray, B., Ghosh, P., Griffith, J., Geuze, H.J. & Kornfeld, S. Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 297, 1700-1703 (2002).
12. Zhdankina, O., Strand, N.L., Redmond, J.M. & Boman, A.L. Yeast GGA proteins interact with GTP-bound Arf and facilitate transport through the Golgi. Yeast 18, 1-18 (2001).
13. Puertollano, R., Randazzo, P.A., Presley, J.F., Hartnell, L.M. & Bonifacino, J.S. The GGAs promote ARF-dependent recruitment of clathrin to the TGN. Cell 105, 93-102 (2001).
14. Takatsu, H., Yoshino, K., Toda, K. & Nakayama, K. GGA proteins associate with Golgi membranes through interaction between their GGAH domains and ADPribosylation factors. Biochem. J. 365, 369-378 (2002).
15. 2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055 (2001).
16. Mao, Y., Chen, J., Maynard, J.A., Zhang, B. & Quiocho, F.A. A novel all helix fold of the AP180 amino-terminal domain for phosphoinositide binding and clathrin assembly in the synaptic vesicle endocytosis. Cell 104, 433-440 (2001).
17. Misra, S., Puertollano, R., Kato, Y., Bonifacino, J.S. & Hurley, J.H. Structural basis for acidic-cluster-dileucine sorting-signal recognition by VHS domains. Nature 415, 933-937 (2002).
18. Shiba, T. et al. Structural basis for recognition of acidic-cluster dileucine sequence by GGA1. Nature 415, 937-941 (2002).
19. Kuai, J., Boman, A.L., Arnold, R.S., Zhu, X. & Kahn, R.A. Effects of activated ADPribosylation factors on Golgi morphology require neither activation of phospholipase D1 nor recruitment of coatomer. J. Biol. Chem. 275, 4022-4032 (2000).
20. Goldberg, J. Structural and function analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 96, 893-902 (1999).
21. Goldberg, J. Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell 95, 237-248 (1998).
22. Jacques, K.M. et al. Arf1 dissociates from the clathrin adaptor GGA prior to being inactivated by Arf GTPase-activating proteins, J. Biol. Chem. 277, 47235-47241 (2002).
23. Hanzal-Bayer, M., Renault, L., Roversi, P. Wittinghofer, A. & Hillig, R.C. The complex of Arl2-GTP and PDEδ: from structure to function. EMBO J. 21, 2095-2106 (2002).
24. Doray, B., Bruns, K., Ghosh, P. & Kornfeld, S. Autoinhibition of the ligand-binding site of GGA1/3 VHS domains by an internal acidic cluster-dileucine motif. Proc. Natl. Acad. Sci. 99, 8072-8077 (2002).
25. Collins, B.M., Watson, P.J. & Owen, D.J. The structure of the GGA1-GAT domain reveals the molecular basis for ARF binding and membrane association of GGAs. Dev. Cell 4, 321-332 (2003).
26. Leslie, A.W.G. Joint CCP4 and ESF-EACMB Newsletter on Protein Crystallography Vol. 26 (Daresbury Laboratory, Warrington, 1992).
27. Evans, P.R. Proceedings of the CCP4 Study Weekend on Data Collection & Processing (eds. Sawyer, L., Isaacs, N. & Bailey, S.) 114-122 (Daresbury Laboratory, Warrington; 1993).
28. Terwilliger, T.C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D 55, 849-861 (1999).
29. Terwilliger, T.C. Maximum-likelihood density modification. Acta Crystallogr. D 56, 965-972 (2000).
30. Perrakis, A., Morris, R. & Lamzin, V.S. Automated protein model building combined with iterative structure refinement. Nature Struct. Biol. 6, 458-463 (1999).
31. Brunger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
32. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255 (1997).
33. Navaza, J. AMoRE - an automated package for molecular replacement. Acta Crystallogr. A 50, 157-163 (1994).
34. Kraulis, P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystaliogr. 24, 946-950 (1991).
35. Merritt, E.A. & Bacon, D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277, 505-524 (1997).
36. Lawrence, M.C. & Bourke, P. CONSCRIPT: a program for generating electron density isosurfaces for presentation in protein crystallography. J. Appl. Crystallogr. 33, 990-991 (2000).
37. Sreerama, N. & Woody, R.W. A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal. Biochem. 209, 32-44 (1993).