Two WXXF-based motifs in NECAPs define the specificity of accessory protein binding to AP-1 and AP-2

EMBO Journal

Volumn 23, Issue 19, 2004, Pages 3701-3710

  Ritter, Brigitte ^a   Denisov, Alexei Yu ^b   Philie, Jacynthe ^a   Deprez, Christophe ^b   Tung, Elaine C ^a   Gehring, Kalle ^b   McPherson, Peter S ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

AAK1; Clathrin; Endocytosis; Stonin; Synaptojanin

Indexed keywords

ADAPTIN ASSOCIATED KINASE 1; ALPHA ADAPTIN; CLATHRIN; CYCLIN G ASSOCIATED KINASE; EPSIN; EPSIN 1; EPSIN 2; NECAP1 PROTEIN; NECAP2 PROTIEN; PROTEIN; STONIN; SYNAPTOJANIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; ENDOCYTOSIS; GOLGI COMPLEX; MEMBRANE VESICLE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; SCREENING;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ADAPTOR PROTEIN COMPLEX GAMMA SUBUNITS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CLATHRIN; DNA-BINDING PROTEINS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; RATS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTOR AP-2; TRANSCRIPTION FACTORS; VESICULAR TRANSPORT PROTEINS;

EID: 6344233187     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600378     Document Type: Article

References (44)

1. Bai H, Doray B, Kornfeld S (2004) GGA1 interacts with the adaptor protein AP-1 through a WNSF sequence in its hinge region. J Biol Chem 279: 17411-17417
2. Barik S (1993) PCR protocols. In Methods in Molecular Biology, Vol. 15, Tolowa: Humana Press Inc
3. Blondeau F, Ritter B, Allaire PD, Wasiak S, Girard M, Hussain NK, Angers A, Legendre-Guillemin V, Roy L, Boismenu D, Kearney RE, Bell AW, Bergeron JJM, McPherson PS (2004) Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc Natl Acad Sci USA 101: 3833-3838
4. Bonifacino JS (2004) The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 5: 23-32
5. Brett TJ, Traub LM, Fremont DH (2002) Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure (Camb) 10: 797-809
6. Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 17: 517-568
7. Collins BM, Praefcke GJ, Robinson MS, Owen DJ (2003) Structural basis for binding of accessory proteins by the appendage domain of GGAs. Nat Struct Biol 10: 607-613
8. Conner SD, Schmid SL (2002) Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J Cell Biol 156: 921-929
9. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422: 37-44
10. Conner SD, Schroter T, Schmid SL (2003) AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin. Traffic 4: 885-890
11. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, Takei K, Daniell L, Nemoto Y, Shears SB, Flavell RA, McCormick DA, De Camilli P (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99: 179-188
12. Denisov AY, Ritter B, McPherson PS, Gehring K (2004) Letter to the Editor: 1H, 15N and 13C resonance assignments and 15N-1H residual dipolar couplings for the alpha-adaptin ear-domain. J Biomol NMR 29: 441-442
13. Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125: 1731-1737
14. Doyle DA, Lee A, Lewis J, Kim E, Sheng M, MacKinnon R (1996) Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85: 1067-1076
15. Drake MT, Traub LM (2001) Interaction of two structurally distinct sequence types with the clathrin terminal domain beta-propeller. J Biol Chem 276: 28700-28709
16. Duncan MC, Costaguta G, Payne GS (2003) Yeast epsin-related proteins required for Golgi-endosome traffic define a gamma-adaptin ear-binding motif. Nat Cell Biol 5: 77-81
17. Hajduk PJ, Gerfin T, Boehlen JM, Haberli M, Marek D, Fesik S (1999) High-throughput nuclear magnetic resonance-based screening. J Med Chem 42: 2315-2317
18. Hinners I, Tooze SA (2003) Changing directions: clathrin-mediated transport between the Golgi and endosomes. J Cell Sci 116: 763-771
19. Jha A, Agostinelli NR, Mishra SK, Keyel PA, Hawryluk MJ, Traub LM (2004) A novel AP-2 adaptor interaction motif initially identified in the long-splice isoform of synaptojanin 1, SJ170. J Biol Chem 279: 2281-2290
20. Kent HM, McMahon HT, Evans PR, Benmerah A, Owen DJ (2002) Gamma-adaptin appendage domain: structure and binding site for Eps15 and gamma-synergin. Structure (Camb) 10: 1139-1148
21. Koradi R, Billeter M, Wuthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55, 29-32
22. Kornau HC, Seeburg PH, Kennedy MB (1997) Interaction of ion channels and receptors with PDZ domain proteins. Curr Opin Neurobiol 7: 368-373
23. Korolchuk VI, Banting G (2002) CK2 and GAK/auxilin2 are major protein kinases in clathrin-coated vesicles. Traffic 3: 428-439
24. Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V (2003) ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J Cell Biol 162: 113-124
25. Mattera R, Arighi CN, Lodge R, Zerial M, Bonifacino JS (2003) Divalent interaction of the GGAs with the Rabaptin-5-Rabex-5 complex. EMBO J 22: 78-88
26. Mattera R, Ritter B, Sidhu SS, McPherson PS, Bonifacino JS (2004) Definition of the consensus motif recognized by {gamma}-adaptin ear domains. J Biol Chem 279: 8018-8028
27. Miele AE, Watson PJ, Evans PR, Traub LM, Owen DJ (2004) Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain beta-propeller. Nat Struct Mol Biol 11: 242-248
28. Miller GJ, Mattera R, Bonifacino JS, Hurley JH (2003) Recognition of accessory protein motifs by the gamma-adaptin ear domain of GGA3. Nat Struct Biol 10: 599-606
29. Nilges M, Macias MJ, O'Donoghue SI, Oschkinat H (1997) Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from beta-spectrin. J Mol Biol 269: 408-422
30. Nogi T, Shiba Y, Kawasaki M, Shiba T, Matsugaki N, Igarashi N, Suzuki M, Kato R, Takatsu H, Nakayama K, Wakatsuki S (2002) Structural basis for the accessory protein recruitment by the gamma-adaptin ear domain. Nat Struct Biol 9: 527-531
31. Owen DJ, Vallis Y, Noble ME, Hunter JB, Dafforn TR, Evans PR, McMahon HT (1999) A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell 97: 805-815
32. Ramjaun AR, McPherson PS (1998) Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J Neurochem 70: 2369-2376
33. Ramjaun AR, Micheva KD, Bouchelet I, McPherson PS (1997) Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J Biol Chem 272: 16700-16706
34. Ritter B, McPherson PS (2004) Molecular mechanisms in clathrin-mediated membrane budding. Topics in Current Genetics, Keränen S, Jantti J (eds), Regulatory Mechanisms of Intracellular Membrane Transport. Springer-Verlag: Berlin, Heidelberg
35. Ritter B, Philie J, Girard M, Tung EC, Blondeau F, McPherson PS (2003) Identification of a family of endocytic proteins that define a new alpha-adaptin ear-binding motif. EMBO Rep 4: 1089-1095
36. Robinson MS (2004) Adaptable adaptors for coated vesicles. Trends Cell Biol 14: 167-174
37. Slepnev VI, Ochoa GC, Butler MH, De Camilli P (2000) Tandem arrangement of the clathrin and AP-2 binding domains in amphiphysin 1 and disruption of clathrin coat function by amphiphysin fragments comprising these sites. J Biol Chem 275: 17583-17589
38. Traub LM, Downs MA, Westrich JL, Fremont DH (1999) Crystal structure of the alpha appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc Natl Acad Sci USA 96: 8907-8912
39. Umeda A, Meyerholz A, Ungewickell E (2000) Identification of the universal cofactor (auxilin 2) in clathrin coat dissociation. Eur J Cell Biol 79: 336-342
40. Walther K, Diril MK, Jung N, Haucke V (2004) Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc Natl Acad Sci USA 101: 964-969
41. Wasiak S, Denisov AY, Han Z, Leventis PA, de Heuvel E, Boulianne GL, Kay BK, Gehring K, McPherson PS (2003) Characterization of a gamma-adaptin ear-binding motif in enthoprotin. FEBS Lett 555: 437-442
42. Wasiak S, Legendre-Guillemin V, Puertollano R, Blondeau F, Girard M, de Heuvel E, Boismenu D, Bell AW, Bonifacino JS, McPherson PS (2002) Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics. J Cell Biol 158: 855-862
43. Wendland B, Emr SD (1998) Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J Cell Biol 141: 71-84
44. Wendland B, Steece KE, Emr SD (1999) Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J 18: 4383-4393