ADP-ribosylation factor 1 transiently activates high-affinity adaptor protein complex AP-1 binding sites on Golgi membranes

Molecular Biology of the Cell

Volumn 9, Issue 6, 1998, Pages 1323-1337

  Zhu, Yunxiang ^a   Traub, Linton M ^a   Kornfeld, Stuart ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE; CLATHRIN;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; RAT; STOICHIOMETRY;

ANIMALIA;

EID: 0031843724     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.6.1323     Document Type: Article

References (77)

1. Ahle, S., Mann, A., Eichelsbacher, U., and Ungewickell, U. (1988). Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J. 7, 919-929.
2. Alconada, A., Bauer, U., and Hoflack, B. (1996). A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localised in the trans-Golgi network. EMBO J. 15, 6096-6110.
3. Antonny, B., Huber, I., Paris, S., Chabre, M., and Cassel, D. (1997). Activation of ADP-ribosylation factor 1 GTPase-activating protein by phosphatydylcholine-derived diacylglycerols. J. Biol. Chem. 272, 30848-30851.
4. Aoe, T., Cukierman, E., Lee, A., Cassel, D., Peters, P.J., and Hsu, V.W. (1997). The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1. EMBO J. 16, 7305-7316.
5. Aridor, M., Bannykh, S.I., Rowe, T., and Balch, W.E. (1995). Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131, 875-893.
6. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M.F., Ravazzola, M., Amherdt, M., and Schekman, R. (1994). COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
7. Bednarek, S.Y., Ravazzola, M., Hosobuchi, M., Amherdt, M., Perrelet, A., Schekman, R., and Orci, L. (1995). COPI- and COPII-coated vesicles bud directly from the endoplasmic reticulum in yeast. Cell 83, 1183-1196.
8. Brodsky, F.M. (1997). New fashions in vesicle coats. Trends Cell Biol. 7, 175-179.
9. Brown, H.A., Gutowski, S., Moomaw, C.R., Slaughter, C., and Sternweis, P.C. (1993). ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75, 1137-1144.
10. Campbell, C., Squicciarini, J., Shia, M., Pilch, P.F., and Fine, R.E. (1984). Identification of a protein kinase as an intrinsic component of rat liver coated vesicles. Biochemistry 23, 4420-4426.
11. Cavenagh, M.M., Whitney, J.A., Carroll, K., Zhang, C., Boman, A.L., Rosenwald, A.G., Mellman, I., and Kahn, R.A. (1996). Intracellular distribution of Arf proteins in mammalian cells: Arf6 is uniquely localized to the plasma membrane. J. Biol. Chem. 271, 21767-21774.
12. Chen, Y.-G., and Shields, D. (1996). ADP-ribosylation factor-1 stimulates formation of nascent secretory vesicles form the trans-Golgi network of endocrine cells. J. Biol. Chem. 271, 5297-5300.
13. Cockcroft, S., Thomas, G.M., Fensome, A., Geny, B., Cunningham, E., Gout, I., Hiles, I., Totty, N.F., Truong, O., and Hsuan, J.J. (1994). Phospholipase D: a downstream effector of ARF in granulocytes. Science 263, 523-526.
14. Damke, H., Baba, T., Warnock, D.E., and Schmid, S.L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
15. Davis, C.G., Lehrman, M.A., Russell, D.W., Anderson, R.G., Brown, M.S., and Goldstein, J.L. (1986). The J.D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 45, 15-24.
16. Dittie, A.S., Hajibagheri, N., and Tooze, S.A. (1996). The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP-ribosylation factor. J. Cell Biol. 132, 523-536.
17. Donaldson, J.G., Finazzi, D., and Klausner, R.D. (1992). Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360, 350-352.
18. Duronio, R.J., Jackson-Machelski, E., Heuckeroth, R.O., Olins, P.O., Devine, C.S., Yonemoto, W., Slice, L.W., Taylor, S.S., and Gordon, J.I. (1990). Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc. Natl. Acad. Sci. USA 87, 1506-1510.
19. Finazzi, D., Cassel, D., Donaldson, J.G., and Klausner, R.D. (1994). Aluminum fluoride acts on the reversibility of ARF1-dependent coat protein binding to Golgi membranes. J. Biol. Chem. 269, 13325-13330.
20. Gaynor, E.C., and Emr, S.D. (1997). COPI-independent anterograde transport: cargo-selective ER to Golgi protein transport in yeast COPI mutants. J. Cell Biol. 136, 789-802.
21. Helms, J.B., Palmer, D.J., and Rothman, J.E. (1993). Two distinct populations of ARF bound to Golgi membranes. J. Cell Biol. 121, 751-760.
22. Helms, J.B., and Rothman, J.E. (1992). Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360, 352-354.
23. Henley, J.R., and McNiven, M.A. (1996). Association of a dynamin-like protein with the Golgi apparatus in mammalian cells. J. Cell Biol. 133, 761-775.
24. Hinshaw, J.E., and Schmid, S.L. (1995). Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374, 190-192.
25. Jadot, M., Canfield, W.M., Gregory, W., and Kornfeld, S. (1992). Characterization of the signal for rapid internalization of the bovine mannose 6-phosphate/insulin-like growth factor-II receptor. J. Biol. Chem. 267, 11069-11077.
26. Kedersha, N.L., and Rome, L.H. (1986). Isolation and characterization of a novel ribonucleoprotein: large structures contain a single species of small RNA. J. Cell Biol. 103, 699-709.
27. Keen, J.H., Willingham, M.C., and Pastan, I.H. (1979). Clathrin-coated vesicles: isolation, dissociation and factor-dependent reassociation of clathrin baskets. Cell 16, 303-312.
28. Kirchhausen, T., Bonifacino, J.S., and Riezman, H. (1997). Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9, 488-495.
29. Kornfeld, S., and Mellman, I. (1989). The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5, 483-525.
30. Le Borgne, R., Griffiths, G., and Hoflack, B. (1996). Mannose 6-phosphate receptors and ADP-ribosylation factors cooperate for high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271, 2162-2170.
31. Le Borgne, R., and Hoflack, B. (1997). Mannose 6-phosphate receptors regulate the formation of clathrin-coated vesicles in the TGN. J. Cell Biol. 137, 335-345.
32. Le Borgne, R., Schmidt, A., Mauxion, F., Griffiths, G., and Hoflack, B. (1993). Binding of AP-1 Golgi adaptors to membranes requires phosphorylated cytoplasmic domains of the mannose 6-phosphate/ insulin-like growth factor II receptor. J. Biol. Chem. 268, 22552-22556.
33. Lenhard, J.M., Kahn, R.A., and Stahl, P.D. (1992). Evidence for ADP-ribosylation factor (ARF) as a regulator of in vitro endosome-endosome fusion. J. Biol. Chem. 267, 13047-13052.
34. Liang, J.O., and Kornfeld, S. (1997). Comparative activity of ADP-ribosylation factor family members in the early steps of coated vesicle formation on rat liver Golgi membranes. J. Biol. Chem. 272, 4141-4148.
35. Liang, J.O., Sung, T.-C., Morris, A.J., Frihman, M.A., and Kornfeld, S. (1997). Different domains of mammalian ADP-ribosylation factor 1 mediate interaction with selected target proteins. J. Biol. Chem. 272, 33001-33008.
36. Ludwig, T., Le Borgne, R., and Hoflack, B. (1995). Roles for mannose 6-phosphate receptors in lysosomal enzyme sorting, IGF-II binding and clathrin-coat assembly. Trends Cell Biol. 5, 202-206.
37. Makler, V., Cukierman, E.M.R., Admon, A., and Cassel, D. (1995). ADP-ribosylation factor-directed GTPase-activating protein: purification and partial characterization. J. Biol. Chem. 270, 5232-5237.
38. Mauxion, F., Le Borgne, R., Munier-Lehmann, H., and Hoflack, B. (1996). A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271, 2171-2178.
39. Mittal, R., Ahmadian, M.R., Goody, R.S., and Wittinghofer, A. (1996). Formation of a transition-state analog of the Ras GTPase reaction by Ras·GDP, tetrafluoroaluminate and GTPase-activating proteins. Science 273, 115-117.
40. Nathke, I.S., Heuser, J., Lupas, A., Stock, J., Turck, C.W., and Brodsky, F.M. (1992). Folding and trimerization of clathrin subunits at the triskelion hub. Cell 68, 899-910.
41. Nixon, A.E., Brune, M., Lowe, P.N., and Webb, M.R. (1995). Kinetics of inorganic phosphate release during the interaction of p21ras with the GTPase-activating proteins, p120GAP and neurofibromin. Biochemistry 34, 15592-15598.
42. Ohno, H., Fournier, M.C., Poy, G., and Bonifacino, J.S. (1996). Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J. BIol. Chem. 271, 29009-29015.
43. Ohno, H.J.S., Fournier, M.-C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Galluser, A., Kirchhausen, T., and Bonifacino, J.S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
44. Orci, L., Stamnes, M., Ravazzola, M., Amherdt, M., Perrelet, A., Sollner, T.H., and Rothman, J.E. (1997). Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335-349.
45. Osterman, J., Orci, L., Tani, K., Amhert, M., Ravazzola, M., Elazar, Z., and Rothman, J.E. (1993). Stepwise assembly of functionally active transport vesicles. Cell 75, 1015-1025.
46. Randazzo, P.A. (1997). Resolution of two ADP-ribosylation factor 1 GTPase-activating proteins from rat liver. Biochem. J. 324, 413-419.
47. Rapoport, I., Miyazaki, M., Boll, W., Duckworth, B., Cantley, L.C., Shoelson, S., and Kirchhausen, T. (1997). Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J. 16, 2240-2250.
48. Rittinger, K., Walker, P.A., Eccleston, J.F., Smerdon, S.J., and Gamblin, S.J. (1997). Structure at1.65 Angstrom of rhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389, 758-762.
49. Robinson, M.S. (1987). 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J. Cell Biol. 104, 887-895.
50. Robinson, M.S. (1994). The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6, 538-544.
51. Robinson, M.S., and Kreis, T.E. (1992). Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell 69, 129-138.
52. Roth, M.G., and Sternweis, P.C. (1997). The role of lipid signaling in constitutive membrane traffic. Curr. Opin. Cell Biol. 9, 519-526.
53. Rothman, J.E. (1994). Mechanisms of intracellular protein transport. Nature 372, 55-63.
54. Salamero, J., Le Borgne, R., Saudrais, C., Goud, B., and Hoflack, B. (1996). Expression of major histocompatibility complex class II molecules in HeLa cells promotes the recruitment of AP-1 Golgi-specific assembly proteins on Golgi membranes. J. Biol. Chem. 273, 30318-30321.
55. Scheffzek, K., Ahmadian, M.R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997). The Ras-Ras GAP complex: structural basis for GTPase activation and ist loss in oncogenic mutants. Science 277, 333-338.
56. Schekman, R., and Orci, L. (1996). Coat proteins and vesicle budding. Science 271, 1526-1533.
57. Schmid, S.L. (1997). Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548.
58. Seaman, M.N.J., Ball, C.L., and Robinson, M.S. (1993). Targeting and mistargeting of plasma membrane adaptors in vitro. J. Cell Biol. 223, 1093-1105.
59. Serafini, T., Orci, L., Amherdt, M., Brunner, M., Kahn, R.A., and Rothman, J.E. (1991). ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell 67, 239-253.
60. Shupliakov, O., Low, P., Grabs, D., Gad, H., Chen, H., David, C., Takei, K., De Camilli, P., and Brodin, L. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263.
61. Simon, J.P., Ivanov, I.E., Shopsin, B., Hersh, D., Adesnik, M., and Sabatini, D.D. (1996). The in vitro generation of post-Golgi vesicles carrying viral envelope glycoproteins requires an ARF-like GTP-binding protein and protein kinase C associated with the Golgi apparatus. J. Biol. Chem. 271, 16952-16961.
62. Stamnes, M.A., and Rothman, J.E. (1993). The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell 73, 999-1005.
63. Tabas, I., and Kornfeld, S. (1979). Purification and characterization of a rat liver Golgi alpha-mannosidase capable of processing asparagine-linked oligosaccharides. J. Biol. Chem. 254, 11655-11663.
64. Takei, K., McPherson, P.S., Schmid, S.L., and De Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature 374, 186-190.
65. Takei, K., Mundigl, O., Daniell, L., and De Camilli, P. (1996). The synaptic vesicle cycle: a single budding step involving clathrin and dynamin. J. Cell Biol. 133, 1237-1250.
66. Tanigawa, G., Orci, L., Amherdt, M., Ravazzola, M., Helms, J.B., and Rothman, J.E. (1993). Hydrolysis of bound GTP by ARF protein triggers uncoating of Golgi-derived COP-coated vesicles. J. Cell Biol. 123, 1365-1371.
67. Teal, S.B., Hsu, V.W., Peters, P.J., Klausner, R.D., and Donaldson, J.G. (1994). An activating mutation in ARF1 stabilizes coatomer binding to Golgi membranes. J. Biol. Chem. 269, 3135-3138.
68. Traub, L.M., Bannykh, S.I., Rodel, J.E., Aridor, M., Balch, W.E., and Kornfeld, S. (1996). AP-2-containing clathrin coats assemble on mature lysosomes. J. Cell Biol. 135, 1801-1804.
69. Traub, L.M., and Kornfeld, S. (1997). The trans-Golgi network: a late secretory sorting station. Curr. Opin. Cell Biol. 9, 527-533.
70. Traub, L.M., Kornfeld, S., and Ungewickell, E. (1995). Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment. J. Biol. Chem. 270, 4933-4942.
71. Traub, L.M., Ostrom, J.A., and Kornfeld, S. (1993). Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol. 123, 561-573.
72. Urrutia, R., Henley, J.R., Cook, T., and McNiven, M.A. (1997). The dynamins: redundant or distinct functions for an expanding family of related GTPases? Proc. Natl. Acad. Sci. USA 94, 377-384.
73. Weiss, O., Holden, J., Rulka, C., and Kahn, R.A. (1989). Nucleotide binding and cofactor activities of purified bovine brain and bacterially expressed ADP-ribosylation factor. J. Biol. Chem. 264, 21066-21072.
74. Wessel, D., and Flugge, U.I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143.
75. West, M.A., Bright, N.A., and Robinson, M.S. (1997). The role of ADP-ribosylation factor and phospholipase D in adaptor recruitment. J. Cell Biol. 138, 1239-1254.
76. Wigge, P., Vallis, Y., and Mcmahon, H.T. (1997). Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr. Biol. 7, 554-560.
77. Wong, D.H., and Brodsky, P.M. (1992). 100-kD proteins of Golgi- and trans-Golgi network-associated coated vesicles have related but distinct membrane binding properties. J. Cell Biol. 117, 1171-1179.