Arf GAPs: Gatekeepers of vesicle generation

FEBS Letters

Volumn 584, Issue 12, 2010, Pages 2646-2651

  Spang, Anne ^a   Shiba, Yoko ^b   Randazzo, Paul A ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Arf GAP; GTPase activating protein; Intracellular traffic; Small GTPase; Vesicle formation

Indexed keywords

ARF PROTEIN; FUNGAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 2; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 3; GUANOSINE TRIPHOSPHATE; PROTEIN GCS1P; PROTEIN GLO3P; UNCLASSIFIED DRUG;

BINDING AFFINITY; CELL MATURATION; CELL MEMBRANE TRANSPORT; CELL VACUOLE; HUMAN; HYDROLYSIS; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTEIN VARIANT; REGULATORY MECHANISM; REVIEW; SEQUENCE HOMOLOGY; YEAST;

ADP-RIBOSYLATION FACTORS; ANIMALS; CYTOPLASMIC VESICLES; GTPASE-ACTIVATING PROTEINS; HUMANS; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77953138522     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.04.005     Document Type: Review

References (61)

1. Randazzo P.A., Kahn R.A. GTP hydrolysis by ADP-ribosylation factor is dependent on both an ADP-ribosylation factor GTPase-activating protein and acid phospholipids. J. Biol. Chem. 1994, 269:10758-10763.
2. Makler V., Cukierman E., Rotman M., Admon A., Cassel D. ADP-ribosylation factor-directed GTPase-activating protein. Purification and partial characterization. J. Biol. Chem. 1995, 270:5232-5237.
3. Cukierman E., Huber I., Rotman M., Cassel D. The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization. Science 1995, 270:1999-2002.
4. Poon P.P., Wang X., Rotman M., Huber I., Cukierman E., Cassel D., Singer R.A., Johnston G.C. Saccharomyces cerevisiae Gcs1 is an ADP-ribosylation factor GTPase-activating protein. Proc. Natl. Acad. Sci. USA 1996, 93:10074-10077.
5. Drebot M.A., Johnston G.C., Singer R.A. A yeast mutant conditionally defective only for reentry into the mitotic cell cycle from stationary phase. Proc. Natl. Acad. Sci. USA 1987, 84:7948-7952.
6. Poon P.P., Cassel D., Spang A., Rotman M., Pick E., Singer R.A., Johnston G.C. Retrograde transport from the yeast Golgi is mediated by two ARF GAP proteins with overlapping function. EMBO J. 1999, 18:555-564.
7. Goldberg J. Structural and functional analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 1999, 96:893-902.
8. Mandiyan V., Andreev J., Schlessinger J., Hubbard S.R. Crystal structure of the ARF-GAP domain and ankyrin repeats of PYK2-associated protein beta. EMBO J. 1999, 18:6890-6898.
9. Randazzo P.A., Terui T., Sturch S., Fales H.M., Ferrige A.G., Kahn R.A. The myristoylated amino terminus of ADP-ribosylation factor 1 is a phospholipid- and GTP-sensitive switch. J. Biol. Chem. 1995, 270:14809-14815.
10. Randazzo P.A., Yang Y.C., Rulka C., Kahn R.A. Activation of ADP-ribosylation factor by Golgi membranes. Evidence for a brefeldin A- and protease-sensitive activating factor on Golgi membranes. J. Biol. Chem. 1993, 268:9555-9563.
11. Scheffzek K., Ahmadian M.R., Wittinghofer A. GTPase-activating proteins: helping hands to complement an active site. Trends Biochem. Sci. 1998, 23:257-262.
12. Kahn R.A., et al. Consensus nomenclature for the human ArfGAP domain-containing proteins. J. Cell Biol. 2008, 182:1039-1044.
13. Inoue H., Randazzo P.A. Arf GAPs and their interacting proteins. Traffic 2007, 8:1465-1475.
14. Bharti S., et al. Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol. Cell Biol. 2007, 27:8271-8283.
15. Hashimoto S., et al. A novel mode of action of an ArfGAP, AMAP2/PAG3/Papa lpha, in Arf6 function. J. Biol. Chem. 2004, 279:37677-37684.
16. Gillingham A.K., Munro S. The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 2007, 23:579-611.
17. Nie Z., Randazzo P.A. Arf GAPs and membrane traffic. J. Cell Sci. 2006, 119:1203-1211.
18. Spang A. ARF1 regulatory factors and COPI vesicle formation. Curr. Opin. Cell Biol. 2002, 14:423-427.
19. Goldberg J. Decoding of sorting signals by coatomer through a GTPase switch in the COPI coat complex. Cell 2000, 100:671-679.
20. Weiss M., Nilsson T. A kinetic proof-reading mechanism for protein sorting. Traffic 2003, 4:65-73.
21. Lee S.Y., Yang J.S., Hong W., Premont R.T., Hsu V.W. ARFGAP1 plays a central role in coupling COPI cargo sorting with vesicle formation. J. Cell Biol. 2005, 168:281-290.
22. Yang J.S., Lee S.Y., Gao M., Bourgoin S., Randazzo P.A., Premont R.T., Hsu V.W. ARFGAP1 promotes the formation of COPI vesicles, suggesting function as a component of the coat. J. Cell Biol. 2002, 159:69-78.
23. Bigay J., Casella J.F., Drin G., Mesmin B., Antonny B. ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J. 2005, 24:2244-2253.
24. Bigay J., Gounon P., Robineau S., Antonny B. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature 2003, 426:563-566.
25. Drin G., Casella J.F., Gautier R., Boehmer T., Schwartz T.U., Antonny B. A general amphipathic alpha-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 2007, 14:138-146.
26. Mesmin B., Drin G., Levi S., Rawet M., Cassel D., Bigay J., Antonny B. Two lipid-packing sensor motifs contribute to the sensitivity of ArfGAP1 to membrane curvature. Biochemistry 2007, 46:1779-1790.
27. Yang J.S., et al. A role for BARS at the fission step of COPI vesicle formation from Golgi membrane. EMBO J. 2005, 24:4133-4143.
28. Manneville J.B., et al. COPI coat assembly occurs on liquid-disordered domains and the associated membrane deformations are limited by membrane tension. Proc. Natl. Acad. Sci. USA 2008, 105:16946-16951.
29. Bremser M., et al. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell 1999, 96:495-506.
30. Nickel W., Brugger B., Wieland F.T. Vesicular transport: the core machinery of COPI recruitment and budding. J. Cell Sci. 2002, 115:3235-3240.
31. Nickel W., Wieland F.T. Biogenesis of COPI-coated transport vesicles. FEBS Lett. 1997, 413:395-400.
32. Rothman J.E. Lasker Basic Medical Research Award. The machinery and principles of vesicle transport in the cell. Nat. Med. 2002, 8:1059-1062.
33. Springer S., Spang A., Schekman R. A primer on vesicle budding. Cell 1999, 97:145-148.
34. Jian X., Brown P., Schuck P., Gruschus J.M., Balbo A., Hinshaw J.E., Randazzo P.A. Autoinhibition of Arf GTPase-activating protein activity by the BAR domain in ASAP1. J. Biol. Chem. 2009, 284:1652-1663.
35. Nie Z., et al. A BAR domain in the N terminus of the Arf GAP ASAP1 affects membrane structure and trafficking of epidermal growth factor receptor. Curr. Biol. 2006, 16:130-139.
36. Gallop J.L., McMahon H.T. BAR domains and membrane curvature: bringing your curves to the BAR. Biochem. Soc. Symp. 2005, 223:31.
37. McMahon H.T., Gallop J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 2005, 438:590-596.
38. Peter B.J., Kent H.M., Mills I.G., Vallis Y., Butler P.J., Evans P.R., McMahon H.T. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 2004, 303:495-499.
39. Luo R., Randazzo P.A. Kinetic analysis of Arf GAP1 indicates a regulatory role for coatomer. J. Biol. Chem. 2008, 283:21965-21977.
40. Luo R., Ha V.L., Hayashi R., Randazzo P.A. Arf GAP2 is positively regulated by coatomer and cargo. Cell Signal. 2009, 21:1169-1179.
41. Frigerio G., Grimsey N., Dale M., Majoul I., Duden R. Two human ARFGAPs associated with COP-I-coated vesicles. Traffic 2007, 8:1644-1655.
42. Kliouchnikov L., Bigay J., Mesmin B., Parnis A., Rawet M., Goldfeder N., Antonny B., Cassel D. Discrete determinants in ArfGAP2/3 conferring Golgi localization and regulation by the COPI coat. Mol. Biol. Cell 2009, 20:859-869.
43. Weimer C., Beck R., Eckert P., Reckmann I., Moelleken J., Brugger B., Wieland F. Differential roles of ArfGAP1, ArfGAP2, and ArfGAP3 in COPI trafficking. J. Cell Biol. 2008, 183:725-735.
44. Szafer E., Pick E., Rotman M., Zuck S., Huber I., Cassel D. Role of coatomer and phospholipids in GTPase-activating protein-dependent hydrolysis of GTP by ADP-ribosylation factor-1. J. Biol. Chem. 2000, 275:23615-23619.
45. Lee I., Doray B., Govero J., Kornfeld S. Binding of cargo sorting signals to AP-1 enhances its association with ADP ribosylation factor 1-GTP. J. Cell Biol. 2008, 180:467-472.
46. Zhu Y., Drake M.T., Kornfeld S. ADP-ribosylation factor 1 dependent clathrin-coat assembly on synthetic liposomes. Proc. Natl. Acad. Sci. USA 1999, 96:5013-5018.
47. Zhu Y., Traub L.M., Kornfeld S. ADP-ribosylation factor 1 transiently activates high-affinity adaptor protein complex AP-1 binding sites on Golgi membranes. Mol. Biol. Cell 1998, 9:1323-1337.
48. Lanoix J., Ouwendijk J., Lin C.C., Stark A., Love H.D., Ostermann J., Nilsson T. GTP hydrolysis by arf-1 mediates sorting and concentration of Golgi resident enzymes into functional COP I vesicles. EMBO J. 1999, 18:4935-4948.
49. Nickel W., Malsam J., Gorgas K., Ravazzola M., Jenne N., Helms J.B., Wieland F.T. Uptake by COPI-coated vesicles of both anterograde and retrograde cargo is inhibited by GTPgammaS in vitro. J. Cell Sci. 1998, 111:3081-3090.
50. Pepperkok R., Whitney J.A., Gomez M., Kreis T.E. COPI vesicles accumulating in the presence of a GTP restricted arf1 mutant are depleted of anterograde and retrograde cargo. J. Cell Sci. 2000, 113:135-144.
51. Saitoh A., Shin H.W., Yamada A., Waguri S., Nakayama K. Three homologous ArfGAPs participate in coat protein I-mediated transport. J. Biol. Chem. 2009, 284:13948-13957.
52. Zhang C.J., Bowzard J.B., Anido A., Kahn R.A. Four ARF GAPs in Saccharomyces cerevisiae have both overlapping and distinct functions. Yeast 2003, 20:315-330.
53. Zhang C.J., Cavenagh M.M., Kahn R.A. A family of Arf effectors defined as suppressors of the loss of Arf function in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 1998, 273:19792-19796.
54. Rein U., Andag U., Duden R., Schmitt H.D., Spang A. ARF-GAP-mediated interaction between the ER-Golgi v-SNAREs and the COPI coat. J. Cell Biol. 2002, 157:395-404.
55. Schindler C., Rodriguez F., Poon P.P., Singer R.A., Johnston G.C., Spang A. The GAP domain and the SNARE, coatomer and cargo interaction region of the ArfGAP2/3 Glo3 are sufficient for Glo3 function. Traffic (Copenhagen, Denmark) 2009, 10:1362-1375.
56. Schindler C., Spang A. Interaction of SNAREs with ArfGAPs precedes recruitment of Sec18p/NSF. Mol. Biol. Cell 2007, 18:2852-2863.
57. Aguilera-Romero A., Kaminska J., Spang A., Riezman H., Muniz M. The yeast p24 complex is required for the formation of COPI retrograde transport vesicles from the Golgi apparatus. J. Cell Biol. 2008, 180:713-720.
58. Sandmann T., Herrmann J.M., Dengjel J., Schwarz H., Spang A. Suppression of coatomer mutants by a new protein family with COPI and COPII binding motifs in Saccharomyces cerevisiae. Mol. Biol. Cell 2003, 14:3097-3113.
59. Lewis S.M., Poon P.P., Singer R.A., Johnston G.C., Spang A. The ArfGAP Glo3 is required for the generation of COPI vesicles. Mol. Biol. Cell 2004, 14:14.
60. Yahara N., Sato K., Nakano A. The Arf1p GTPase-activating protein Glo3p executes its regulatory function through a conserved repeat motif at its C-terminus. J. Cell Sci. 2006, 119:2604-2612.
61. Poon P.P., Nothwehr S.F., Singer R.A., Johnston G.C. The Gcs1 and Age2 ArfGAP proteins provide overlapping essential function for transport from the yeast trans-Golgi network. J. Cell Biol. 2001, 155:1239-1250.