Molecular Basis for the Sorting of the SNARE VAMP7 into Endocytic Clathrin-Coated Vesicles by the ArfGAP Hrb

Cell

Volumn 134, Issue 5, 2008, Pages 817-827

  Pryor, Paul R ^a   Jackson, Lauren ^b   Gray, Sally R ^a   Edeling, Melissa A ^a   Thompson, Amanda ^c   Sanderson, Christopher M ^c   Evans, Philip R ^b   Owen, David J ^a   Luzio, J Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

CELLBIO; PROTEINS; SIGNALING

Indexed keywords

ADAPTOR PROTEIN; ARF PROTEIN; ARFGAP PROTEIN; CLATHRIN; HRB PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG; VESICLE ASSOCIATED MEMBRANE PROTEIN 7;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CELL VACUOLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT;

EID: 50549086057     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.07.023     Document Type: Article

References (40)

1. Bonifacino J.S., and Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72 (2003) 395-447
2. Bowers K., Lottridge J., Helliwell S.B., Goldthwaite L.M., Luzio J.P., and Stevens T.H. Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae. Traffic 5 (2004) 194-210
3. Chen Y.A., and Scheller R.H. SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2 (2001) 98-106
4. Collins B.M., McCoy A.J., Kent H.M., Evans P.R., and Owen D.J. Molecular architecture and functional model of the endocytic AP2 complex. Cell 109 (2002) 523-535
5. Cuff J.A., Clamp M.E., Siddiqui A.S., Finlay M., and Barton G.J. JPred: a consensus secondary structure prediction server. Bioinformatics 14 (1998) 892-893
6. Doria M., Salcini A.E., Colombo E., Parslow T.G., Pelicci P.G., and Di Fiore P.P. The eps15 homology (EH) domain-based interaction between eps15 and hrb connects the molecular machinery of endocytosis to that of nucleocytosolic transport. J. Cell Biol. 147 (1999) 1379-1384
7. Edeling M.A., Mishra S.K., Keyel P.A., Steinhauser A.L., Collins B.M., Roth R., Heuser J.E., Owen D.J., and Traub L.M. Molecular switches involving the AP-2 β2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell 10 (2006) 329-342
8. Fasshauer D., Sutton R.B., Brunger A.T., and Jahn R. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. USA 95 (1998) 15781-15786
9. Filippini F., Rossi V., Galli T., Budillon A., D'Urso M., and D'Esposito M. Longins: a new evolutionary conserved VAMP family sharing a novel SNARE domain. Trends Biochem. Sci. 26 (2001) 407-409
10. French A.P., Mills S., Swarup R., Bennett M.J., and Pridmore T.P. Colocalization of fluorescent markers in confocal microscope images of plant cells. Nat. Protoc. 3 (2008) 619-628
11. Fritz C.C., Zapp M.L., and Green M.R. A human nucleoporin-like protein that specifically interacts with HIV Rev. Nature 376 (1995) 530-533
12. Gonzalez Jr. L.C., Weis W.I., and Scheller R.H. A novel SNARE N-terminal domain revealed by the crystal structure of Sec22b. J. Biol. Chem. 276 (2001) 24203-24211
13. Hirst J., Miller S.E., Taylor M.J., von Mollard G.F., and Robinson M.S. EpsinR is an adaptor for the SNARE protein Vti1b. Mol. Biol. Cell 15 (2004) 5593-5602
14. Hong W. SNAREs and traffic. Biochim. Biophys. Acta 1744 (2005) 493-517
15. James P., Halladay J., and Craig E.A. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144 (1996) 1425-1436
16. Krissinel E., and Henrick K. Detection of Protein Assemblies in Crystals (2005), Springer-Verlag, Berlin, Heidelberg
17. Lehner B., Semple J.I., Brown S.E., Counsell D., Campbell R.D., and Sanderson C.M. Analysis of a high-throughput yeast two-hybrid system and its use to predict the function of intracellular proteins encoded within the human MHC class III region. Genomics 83 (2004) 153-167
18. Liu Y., Flanagan J.J., and Barlowe C. Sec22p export from the endoplasmic reticulum is independent of SNARE pairing. J. Biol. Chem. 279 (2004) 27225-27232
19. Luzio J.P., Pryor P.R., and Bright N.A. Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8 (2007) 622-632
20. Mancias J.D., and Goldberg J. The transport signal on Sec22 for packaging into COPII-coated vesicles is a conformational epitope. Mol. Cell 26 (2007) 403-414
21. Martinez-Arca S., Alberts P., Zahraoui A., Louvard D., and Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J. Cell Biol. 149 (2000) 889-900
22. Martinez-Arca S., Proux-Gillardeaux V., Alberts P., Louvard D., and Galli T. Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J. Cell Sci. 116 (2003) 2805-2816
23. Martinez-Arca S., Rudge R., Vacca M., Raposo G., Camonis J., Proux-Gillardeaux V., Daviet L., Formstecher E., Hamburger A., Filippini F., et al. A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. USA 100 (2003) 9011-9016
24. McNew J.A., Parlati F., Fukuda R., Johnston R.J., Paz K., Paumet F., Sollner T.H., and Rothman J.E. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407 (2000) 153-159
25. Miller S.E., Collins B.M., McCoy A.J., Robinson M.S., and Owen D.J. A SNARE-adaptor interaction is a new mode of cargo recognition in clathrin-coated vesicles. Nature 450 (2007) 570-574
26. Mossessova E., Bickford L.C., and Goldberg J. SNARE selectivity of the COPII coat. Cell 114 (2003) 483-495
27. Peden A.A., Oorschot V., Hesser B.A., Austin C.D., Scheller R.H., and Klumperman J. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 164 (2004) 1065-1076
28. Pelham H.R. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 11 (2001) 99-101
29. Praefcke G.J., Ford M.G., Schmid E.M., Olesen L.E., Gallop J.L., Peak-Chew S.Y., Vallis Y., Babu M.M., Mills I.G., and McMahon H.T. Evolving nature of the AP2 α-appendage hub during clathrin-coated vesicle endocytosis. EMBO J. 23 (2004) 4371-4383
30. Pryor P.R., Mullock B.M., Bright N.A., Lindsay M.R., Gray S.R., Richardson S.C., Stewart A., James D.E., Piper R.C., and Luzio J.P. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 5 (2004) 590-595
31. Rao S.K., Huynh C., Proux-Gillardeaux V., Galli T., and Andrews N.W. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J. Biol. Chem. 279 (2004) 20471-20479
32. Reaves B.J., Bright N.A., Mullock B.M., and Luzio J.P. The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J. Cell Sci. 109 (1996) 749-762
33. Reid E., Connell J., Edwards T.L., Duley S., Brown S.E., and Sanderson C.M. The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum. Mol. Genet. 14 (2005) 19-38
34. 2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137 (1997) 93-104
35. Schmid E.M., and McMahon H.T. Integrating molecular and network biology to decode endocytosis. Nature 448 (2007) 883-888
36. Schmid E.M., Ford M.G., Burtey A., Praefcke G.J., Peak-Chew S.Y., Mills I.G., Benmerah A., and McMahon H.T. Role of the AP2 β-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol. 4 (2006) e262
37. Schwartz T., and Blobel G. Structural basis for the function of the β subunit of the eukaryotic signal recognition particle receptor. Cell 112 (2003) 793-803
38. Tochio H., Tsui M.M., Banfield D.K., and Zhang M. An autoinhibitory mechanism for nonsyntaxin SNARE proteins revealed by the structure of Ykt6p. Science 293 (2001) 698-702
39. Wen W., Chen L., Wu H., Sun X., Zhang M., and Banfield D.K. Identification of the yeast R-SNARE Nyv1p as a novel longin domain-containing protein. Mol. Biol. Cell 17 (2006) 4282-4299
40. Yang B., Gonzalez Jr. L., Prekeris R., Steegmaier M., Advani R.J., and Scheller R.H. SNARE interactions are not selective. Implications for membrane fusion specificity. J. Biol. Chem. 274 (1999) 5649-5653