A conformational change in the α-subunit of coatomer induced by ligand binding to γ-COP revealed by single-pair FRET

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Volumn 9, Issue 4, 2008, Pages 597-607

  Langer, Julian D ^a   Roth, Christian M ^a   Béthune, Julien ^a   Stoops, Emily H ^a   Brügger, Britta ^a   Herten, Dirk Peter ^a   Wieland, Felix T ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Coatomer; COPI; Fluorescence resonance energy transfer; p24 proteins; Single molecule spectroscopy

Indexed keywords

COAT PROTEIN; COAT PROTEIN COMPLEX I; COATOMER PROTEIN; FLUORESCENT DYE; GAMMA COAT PROTEIN; LIGAND; MEMBRANE PROTEIN; PROTEIN P23; UNCLASSIFIED DRUG;

ALPHA CHAIN; ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE RESONANCE ENERGY TRANSFER; GOLGI COMPLEX; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN POLYMERIZATION; RAT;

EID: 40449083572     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00697.x     Document Type: Article

References (44)

1. 1 McMahon HT, Mills IG. COP and clathrin‐coated vesicle budding: different pathways, common approaches. Curr Opin Cell Biol 2004 ; 16: 379–391.
2. 2 Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravazzola M, Amherdt M, Schekman R. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 1994 ; 77: 895–907.
3. 3 Kirchhausen T. Clathrin. Annu Rev Biochem 2000 ; 69: 699–727.
4. 4 Waters MG, Serafini T, Rothman JE. ‘Coatomer’: a cytosolic protein complex containing subunits of non‐clathrin‐coated Golgi transport vesicles. Nature 1991 ; 349: 248–251.
5. 5 Serafini T, Stenbeck G, Brecht A, Lottspeich F, Orci L, Rothman JE, Wieland FT. A coat subunit of Golgi‐derived non‐clathrin‐coated vesicles with homology to the clathrin‐coated vesicle coat protein beta‐adaptin. Nature 1991 ; 349: 215–220.
6. 6 Nakano A, Muramatsu M. A novel GTP‐binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J Cell Biol 1989 ; 109: 2677–2691.
7. 7 Barlowe C, D’Enfert C, Schekman R. Purification and characterization of SAR1p, a small GTP‐binding protein required for transport vesicle formation from the endoplasmic reticulum. J Biol Chem 1993 ; 268: 873–879.
8. 8 Serafini T, Orci L, Amherdt M, Brunner M, Kahn RA, Rothman JE. ADP‐ribosylation factor is a subunit of the coat of Golgi‐derived COP‐coated vesicles: a novel role for a GTP‐binding protein. Cell 1991 ; 67: 239–253.
9. 9 Donaldson JG, Cassel D, Kahn RA, Klausner RD. ADP‐ribosylation factor, a small GTP‐binding protein, is required for binding of the coatomer protein beta‐COP to Golgi membranes. Proc Natl Acad Sci U S A 1992 ; 89: 6408–6412.
10. 10 Palmer DJ, Helms JB, Beckers CJ, Orci L, Rothman JE. Binding of coatomer to Golgi membranes requires ADP‐ribosylation factor. J Biol Chem 1993 ; 268: 12083–12089.
11. 11 Austin C, Hinners I, Tooze SA. Direct and GTP‐dependent interaction of ADP‐ribosylation factor 1 with clathrin adaptor protein AP‐1 on immature secretory granules. J Biol Chem 2000 ; 275: 21862–21869.
12. 12 Ooi CE, Dell’Angelica EC, Bonifacino JS. ADP‐Ribosylation factor 1 (ARF1) regulates recruitment of the AP‐3 adaptor complex to membranes. J Cell Biol 1998 ; 142: 391–402.
13. 13 Boehm M, Aguilar RC, Bonifacino JS. Functional and physical interactions of the adaptor protein complex AP‐4 with ADP‐ribosylation factors (ARFs). Embo J 2001 ; 20: 6265–6276.
14. 14 Paleotti O, Macia E, Luton F, Klein S, Partisani M, Chardin P, Kirchhausen T, Franco M. The small G‐protein Arf6GTP recruits the AP‐2 adaptor complex to membranes. J Biol Chem 2005 ; 280: 21661–21666.
15. 15 Hara‐Kuge S, Kuge O, Orci L, Amherdt M, Ravazzola M, Wieland FT, Rothman JE. En bloc incorporation of coatomer subunits during the assembly of COP‐coated vesicles. J Cell Biol 1994 ; 124: 883–892.
16. 16 Letourneur F, Gaynor EC, Hennecke S, Demolliere C, Duden R, Emr SD, Riezman H, Cosson P. Coatomer is essential for retrieval of dilysine‐tagged proteins to the endoplasmic reticulum. Cell 1994 ; 79: 1199–1207.
17. 17 Stamnes MA, Craighead MW, Hoe MH, Lampen N, Geromanos S, Tempst P, Rothman JE. An integral membrane component of coatomer‐coated transport vesicles defines a family of proteins involved in budding. Proc Natl Acad Sci U S A 1995 ; 92: 8011–8015.
18. 18 Sohn K, Orci L, Ravazzola M, Amherdt M, Bremser M, Lottspeich F, Fiedler K, Helms JB, Wieland FT. A major transmembrane protein of Golgi‐derived COPI‐coated vesicles involved in coatomer binding. J Cell Biol 1996 ; 135: 1239–1248.
19. 19 Malsam J, Satoh A, Pelletier L, Warren G. Golgin tethers define subpopulations of COPI vesicles. Science 2005 ; 307: 1095–1098.
20. 20 Reinhard C, Harter C, Bremser M, Brugger B, Sohn K, Helms JB, Wieland F. Receptor‐induced polymerization of coatomer. Proc Natl Acad Sci U S A 1999 ; 96: 1224–1228.
21. 21 Bethune J, Kol M, Hoffmann J, Reckmann I, Brugger B, Wieland F. Coatomer, the coat protein of COPI transport vesicles, discriminates endoplasmic reticulum residents from p24 proteins. Mol Cell Biol 2006 ; 26: 8011–8021.
22. 22 Eugster A, Frigerio G, Dale M, Duden R. The alpha‐ and beta’‐COP WD40 domains mediate cargo‐selective interactions with distinct di‐lysine motifs. Mol Biol Cell 2004 ; 15: 1011–1023.
23. 23 Matsui W, Kirchhausen T. Stabilization of clathrin coats by the core of the clathrin‐associated protein complex AP‐2. Biochemistry 1990 ; 29: 10791–10798.
24. 24 Haucke V, De Camilli P. AP‐2 recruitment to synaptotagmin stimulated by tyrosine‐based endocytic motifs. Science 1999 ; 285: 1268–1271.
25. 25 Boll W, Rapoport I, Brunner C, Modis Y, Prehn S, Kirchhausen T. The mu2 subunit of the clathrin adaptor AP‐2 binds to FDNPVY and YppO sorting signals at distinct sites. Traffic 2002 ; 3: 590–600.
26. 26 Langer JD, Stoops EH, Bethune J, Wieland FT. Conformational changes of coat proteins during vesicle formation. FEBS Lett 2007 ; 581: 2083–2088.
27. 27 Lee JY, Okumus B, Kim DS, Ha T. Extreme conformational diversity in human telomeric DNA. Proc Natl Acad Sci U S A 2005 ; 102: 18938–18943.
28. 28 Ha T, Zhuang X, Kim HD, Orr JW, Williamson JR, Chu S. Ligand‐induced conformational changes observed in single RNA molecules. Proc Natl Acad Sci U S A 1999 ; 96: 9077–9082.
29. 29 Michalet X, Weiss S, Jager M. Single‐molecule fluorescence studies of protein folding and conformational dynamics. Chem Rev 2006 ; 106: 1785–1813.
30. 30 Myong S, Stevens BC, Ha T. Bridging conformational dynamics and function using single‐molecule spectroscopy. Structure 2006 ; 14: 633–643.
31. 31 Wegmann D, Hess P, Baier C, Wieland FT, Reinhard C. Novel isotypic gamma/zeta subunits reveal three coatomer complexes in mammals. Mol Cell Biol 2004 ; 24: 1070–1080.
32. 32 Ha T. Single‐molecule fluorescence resonance energy transfer. Methods 2001 ; 25: 78–86.
33. 33 Deniz AA, Laurence TA, Dahan M, Chemla DS, Schultz PG, Weiss S. Ratiometric single‐molecule studies of freely diffusing biomolecules. Annu Rev Phys Chem 2001 ; 52: 233–253.
34. 34 Pavel J, Harter C, Wieland FT. Reversible dissociation of coatomer: functional characterization of a beta/delta‐coat protein subcomplex. Proc Natl Acad Sci U S A 1998 ; 95: 2140–2145.
35. 35 Eugster A, Frigerio G, Dale M, Duden R. COP I domains required for coatomer integrity, and novel interactions with ARF and ARF‐GAP. EMBO J 2000 ; 19: 3905–3917.
36. 36 Duden R, Griffiths G, Frank R, Argos P, Kreis TE. Beta‐COP, a 110 kd protein associated with non‐clathrin‐coated vesicles and the Golgi complex, shows homology to beta‐adaptin. Cell 1991 ; 64: 649–665.
37. 37 Schledzewski K, Brinkmann H, Mendel RR. Phylogenetic analysis of components of the eukaryotic vesicle transport system reveals a common origin of adaptor protein complexes 1, 2, and 3 and the F subcomplex of the coatomer COPI. J Mol Evol 1999 ; 48: 770–778.
38. 38 Rapoport I, Miyazaki M, Boll W, Duckworth B, Cantley LC, Shoelson S, Kirchhausen T. Regulatory interactions in the recognition of endocytic sorting signals by AP‐2 complexes. EMBO J 1997 ; 16: 2240–2250.
39. 39 Fingerhut A, Von Figura K, Honing S. Binding of AP2 to sorting signals is modulated by AP2 phosphorylation. J Biol Chem 2001 ; 276: 5476–5482.
40. 40 Ricotta D, Conner SD, Schmid SL, Von Figura K, Honing S. Phosphorylation of the AP2 mu subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J Cell Biol 2002 ; 156: 791–795.
41. 41 Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ. Molecular architecture and functional model of the endocytic AP2 complex. Cell 2002 ; 109: 523–535.
42. 42 Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T. Endocytosis by random initiation and stabilization of clathrin‐coated pits. Cell 2004 ; 118: 591–605.
43. 43 Tabas I, Kornfeld S. Purification and characterization of a rat liver Golgi alpha‐mannosidase capable of processing asparagine‐linked oligosaccharides. J Biol Chem 1979 ; 254: 11655–11663.
44. 44 Franco M, Chardin P, Chabre M, Paris S. Myristoylation of ADP‐ribosylation factor 1 facilitates nucleotide exchange at physiological Mg2+ levels. J Biol Chem 1995 ; 270: 1337–1341.