ADP-Ribosylation Factor 1 (ARF1) Regulates Recruitment of the AP-3 Adaptor Complex to Membranes

doi:10.1083/jcb.142.2.391

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© The Rockefeller University Press, 0021-9525/1998//391 $5.00
The Journal of Cell Biology, Volume 142, Number 2, , 1998 391-402

Articles

ADP-Ribosylation Factor 1 (ARF1) Regulates Recruitment of the AP-3 Adaptor Complex to Membranes

Chean Eng Ooi, Esteban C. Dell'Angelica, and Juan S. Bonifacino

Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health (NIH), Bethesda, Maryland 20892

Small GTP-binding proteins such as ADP- ribosylation factor1 (ARF1) and Sar1p regulate the membrane association of coatproteins involved in intracellular membrane trafficking. ARF1controls the clathrin coat adaptor AP-1 and the nonclathrincoat COPI, whereas Sar1p controls the nonclathrin coat COPII.In this study, we demonstrate that membrane association ofthe recently described AP-3 adaptor is regulated by ARF1. Associationof AP-3 with membranes in vitro was enhanced by GTP ${gamma}$ S and inhibited by brefeldin A (BFA), an inhibitor of ARF1 guanine nucleotideexchange. In addition, recombinant myristoylated ARF1 promotedassociation of AP-3 with membranes. The role of ARF1 in vivowas examined by assessing AP-3 subcellular localization whenthe intracellular level of ARF1-GTP was altered through overexpressionof dominant ARF1 mutants or ARF1- GTPase-activating protein(GAP). Lowering ARF1-GTP levels resulted in redistribution ofAP-3 from punctate membrane-bound structures to the cytosolas seen by immunofluorescence microscopy. In contrast, increasingARF1-GTP levels prevented redistribution of AP-3 to the cytosolinduced by BFA or energy depletion. Similar experiments withmutants of ARF5 and ARF6 showed that these other ARF familymembers had little or no effect on AP-3. Taken together, ourresults indicate that membrane recruitment of AP-3 is promotedby ARF1-GTP. This finding suggests that ARF1 is not a regulatorof specific coat proteins, but rather is a ubiquitous molecularswitch that acts as a transducer of diverse signals influencingcoat assembly.

Key Words: ARF • adaptin • coat • endosomes • BFA

Abbreviations used in this paper: AP, adaptor protein; ARF, ADP-ribosylation factor; BFA, brefeldin A; CB, coat-binding; DOG, 2-deoxyglucose; GAP, GTPase-activating protein; GEF, guanine nucleotide exchange factor; HA, hemagglutinin; HB, homogenization buffer; HMW, high molecular weight.

Address all correspondence to Juan S. Bonifacino, Cell Biologyand Metabolism Branch, National Institute of Child Health andHuman Development, Building 18T/Room 101, National Institutesof Health (NIH), Bethesda, MD 20892. Tel.: (301) 496-6368. Fax:(301) 402-0078. E-mail: juan{at}helix.nih.gov

2. The ARF antibody used (clone 1D9) recognizes all five knownhuman ARF proteins, but ARF1 and/or ARF3 is by far the mostabundant ARF species in cells, comprising >90% of totalcellular ARF.

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Newell-Litwa, K., Seong, E., Burmeister, M., Faundez, V. (2007). Neuronal and non-neuronal functions of the AP-3 sorting machinery. J. Cell Sci. 120: 531-541 [Abstract] [Full Text]
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Natsume, W., Tanabe, K., Kon, S., Yoshida, N., Watanabe, T., Torii, T., Satake, M. (2006). SMAP2, a Novel ARF GTPase-activating Protein, Interacts with Clathrin and Clathrin Assembly Protein and Functions on the AP-1-positive Early Endosome/Trans-Golgi Network. Mol. Biol. Cell 17: 2592-2603 [Abstract] [Full Text]
Baust, T., Czupalla, C., Krause, E., Bourel-Bonnet, L., Hoflack, B. (2006). Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc. Natl. Acad. Sci. USA 103: 3159-3164 [Abstract] [Full Text]
Belov, G. A., Fogg, M. H., Ehrenfeld, E. (2005). Poliovirus Proteins Induce Membrane Association of GTPase ADP-Ribosylation Factor. J. Virol. 79: 7207-7216 [Abstract] [Full Text]
LI, Y., KELLY, W. G., LOGSDON, J. M. JR, SCHURKO, A. M., HARFE, B. D., HILL-HARFE, K. L., KAHN, R. A. (2004). Functional genomic analysis of the ADP-ribosylation factor family of GTPases: phylogeny among diverse eukaryotes and function in C. elegans. FASEB J. 18: 1834-1850 [Abstract] [Full Text]
Shin, H.-W., Morinaga, N., Noda, M., Nakayama, K. (2004). BIG2, A Guanine Nucleotide Exchange Factor for ADP-Ribosylation Factors: Its Localization to Recycling Endosomes and Implication in the Endosome Integrity. Mol. Biol. Cell 15: 5283-5294 [Abstract] [Full Text]
Lee, G.-J., Sohn, E. J., Lee, M. H., Hwang, I. (2004). The Arabidopsis Rab5 Homologs Rha1 and Ara7 Localize to the Prevacuolar Compartment. Plant Cell Physiol 45: 1211-1220 [Abstract] [Full Text]
Kalthoff, C., Groos, S., Kohl, R., Mahrhold, S., Ungewickell, E. J. (2002). Clint: A Novel Clathrin-binding ENTH-Domain Protein at the Golgi. Mol. Biol. Cell 13: 4060-4073 [Abstract] [Full Text]
Yang, J.-S., Lee, S. Y., Gao, M., Bourgoin, S., Randazzo, P. A., Premont, R. T., Hsu, V. W. (2002). ARFGAP1 promotes the formation of COPI vesicles, suggesting function as a component of the coat. JCB 159: 69-78 [Abstract] [Full Text]
Hua, Z., Fatheddin, P., Graham, T. R. (2002). An Essential Subfamily of Drs2p-related P-Type ATPases Is Required for Protein Trafficking between Golgi Complex and Endosomal/Vacuolar System. Mol. Biol. Cell 13: 3162-3177 [Abstract] [Full Text]
Yu, S., Roth, M. G. (2002). Casein Kinase I Regulates Membrane Binding by ARF GAP1. Mol. Biol. Cell 13: 2559-2570 [Abstract] [Full Text]
Lee, M. H., Min, M. K., Lee, Y. J., Jin, J. B., Shin, D. H., Kim, D. H., Lee, K.-H., Hwang, I. (2002). ADP-Ribosylation Factor 1 of Arabidopsis Plays a Critical Role in Intracellular Trafficking and Maintenance of Endoplasmic Reticulum Morphology in Arabidopsis. Plant Physiol. 129: 1507-1520 [Abstract] [Full Text]
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Click, E. S., Stearns, T., Botstein, D. (2002). Systematic Structure-Function Analysis of the Small GTPase Arf1 in Yeast. Mol. Biol. Cell 13: 1652-1664 [Abstract] [Full Text]
Lu, L., Horstmann, H., Ng, C., Hong, W. (2002). Regulation of Golgi structure and function by ARF-like protein 1 (Arl1). J. Cell Sci. 114: 4543-4555 [Abstract] [Full Text]
Szafer, E., Rotman, M., Cassel, D. (2001). Regulation of GTP Hydrolysis on ADP-ribosylation Factor-1 at the Golgi Membrane. J. Biol. Chem. 276: 47834-47839 [Abstract] [Full Text]
Claing, A., Chen, W., Miller, W. E., Vitale, N., Moss, J., Premont, R. T., Lefkowitz, R. J. (2001). beta -Arrestin-mediated ADP-ribosylation Factor 6 Activation and beta 2-Adrenergic Receptor Endocytosis. J. Biol. Chem. 276: 42509-42513 [Abstract] [Full Text]
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Mazaki, Y., Hashimoto, S., Okawa, K., Tsubouchi, A., Nakamura, K., Yagi, R., Yano, H., Kondo, A., Iwamatsu, A., Mizoguchi, A., Sabe, H. (2001). An ADP-Ribosylation Factor GTPase-activating Protein Git2-short/KIAA0148 Is Involved in Subcellular Localization of Paxillin and Actin Cytoskeletal Organization. Mol. Biol. Cell 12: 645-662 [Abstract] [Full Text]
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Drake, M. T., Zhu, Y., Kornfeld, S. (2000). The Assembly of AP-3 Adaptor Complex-containing Clathrin-coated Vesicles on Synthetic Liposomes. Mol. Biol. Cell 11: 3723-3736 [Abstract] [Full Text]
Jackson, T. R., Brown, F. D., Nie, Z., Miura, K., Foroni, L., Sun, J., Hsu, V. W., Donaldson, J. G., Randazzo, P. A. (2000). Acaps Are Arf6 Gtpase-Activating Proteins That Function in the Cell Periphery. JCB 151: 627-638 [Abstract] [Full Text]
Okamoto, C. T., McKinney, J., Jeng, Y. Y. (2000). Clathrin in mitotic spindles. Am. J. Physiol. Cell Physiol. 279: C369-C374 [Abstract] [Full Text]
Martin, M. E., Hidalgo, J., Rosa, J. L., Crottet, P., Velasco, A. (2000). Effect of Protein Kinase A Activity on the Association of ADP-ribosylation Factor 1 to Golgi Membranes. J. Biol. Chem. 275: 19050-19059 [Abstract] [Full Text]
Turner, M. D., Arvan, P. (2000). Protein Traffic from the Secretory Pathway to the Endosomal System in Pancreatic beta -Cells. J. Biol. Chem. 275: 14025-14030 [Abstract] [Full Text]
Dell'Angelica, E. C., Puertollano, R., Mullins, C., Aguilar, R. C., Vargas, J. D., Hartnell, L. M., Bonifacino, J. S. (2000). Ggas: A Family of Adp Ribosylation Factor-Binding Proteins Related to Adaptors and Associated with the Golgi Complex. JCB 149: 81-94 [Abstract] [Full Text]
Boman, A. L., Zhang, C.-j., Zhu, X., Kahn, R. A. (2000). A Family of ADP-Ribosylation Factor Effectors That Can Alter Membrane Transport through the trans-Golgi. Mol. Biol. Cell 11: 1241-1255 [Abstract] [Full Text]
Kondo, A., Hashimoto, S., Yano, H., Nagayama, K., Mazaki, Y., Sabe, H. (2000). A New Paxillin-binding Protein, PAG3/Papalpha /KIAA0400, Bearing an ADP-Ribosylation Factor GTPase-activating Protein Activity, Is Involved in Paxillin Recruitment to Focal Adhesions and Cell Migration. Mol. Biol. Cell 11: 1315-1327 [Abstract] [Full Text]
Gu, F., Gruenberg, J. (2000). ARF1 Regulates pH-dependent COP Functions in the Early Endocytic Pathway. J. Biol. Chem. 275: 8154-8160 [Abstract] [Full Text]
Kuai, J., Boman, A. L., Arnold, R. S., Zhu, X., Kahn, R. A. (2000). Effects of Activated ADP-ribosylation Factors on Golgi Morphology Require neither Activation of Phospholipase D1 nor Recruitment of Coatomer. J. Biol. Chem. 275: 4022-4032 [Abstract] [Full Text]
Dell'Angelica, E. C., Aguilar, R. C., Wolins, N., Hazelwood, S., Gahl, W. A., Bonifacino, J. S. (2000). Molecular Characterization of the Protein Encoded by the Hermansky-Pudlak Syndrome Type 1 Gene. J. Biol. Chem. 275: 1300-1306 [Abstract] [Full Text]
Rohn, W., Rouille, Y, Waguri, S, Hoflack, B (2000). Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J. Cell Sci. 113: 2093-2101 [Abstract]
Blagoveshchenskaya, A. D., Hewitt, E. W., Cutler, D. F. (1999). Di-Leucine Signals Mediate Targeting of Tyrosinase and Synaptotagmin to Synaptic-like Microvesicles within PC12 Cells. Mol. Biol. Cell 10: 3979-3990 [Abstract] [Full Text]
Gaschet, J., Hsu, V. W. (1999). Distribution of ARF6 between Membrane and Cytosol Is Regulated by Its GTPase Cycle. J. Biol. Chem. 274: 20040-20045 [Abstract] [Full Text]
Sata, M., Moss, J., Vaughan, M. (1999). Structural basis for the inhibitory effect of brefeldin A on guanine nucleotide-exchange proteins for ADP-ribosylation factors. Proc. Natl. Acad. Sci. USA 96: 2752-2757 [Abstract] [Full Text]
Dell'Angelica, E. C., Mullins, C., Bonifacino, J. S. (1999). AP-4, a Novel Protein Complex Related to Clathrin Adaptors. J. Biol. Chem. 274: 7278-7285 [Abstract] [Full Text]
Zhu, Y., Traub, L. M., Kornfeld, S. (1999). High-Affinity Binding Of The AP-1 Adaptor Complex to Trans-Golgi Network Membranes Devoid Of Mannose 6-Phosphate Receptors. Mol. Biol. Cell 10: 537-549 [Abstract] [Full Text]
Simmen, T, Schmidt, A, Hunziker, W, Beermann, F (1999). The tyrosinase tail mediates sorting to the lysosomal compartment in MDCK cells via a di-leucine and a tyrosine-based signal. J. Cell Sci. 112: 45-53 [Abstract]
Brown, M. T., Andrade, J., Radhakrishna, H., Donaldson, J. G., Cooper, J. A., Randazzo, P. A. (1998). ASAP1, a Phospholipid-Dependent Arf GTPase-Activating Protein That Associates with and Is Phosphorylated by Src. Mol. Cell. Biol. 18: 7038-7051 [Abstract] [Full Text]
Klumperman, J, Schweizer, A, Clausen, H, Tang, B., Hong, W, Oorschot, V, Hauri, H. (1998). The recycling pathway of protein ERGIC-53 and dynamics of the ER-Golgi intermediate compartment. J. Cell Sci. 111: 3411-3425 [Abstract]
Liendo, A., Stedman, T. T., Ngo, H. M., Chaturvedi, S., Hoppe, H. C., Joiner, K. A. (2001). Toxoplasma gondii ADP-ribosylation Factor 1 Mediates Enhanced Release of Constitutively Secreted Dense Granule Proteins. J. Biol. Chem. 276: 18272-18281 [Abstract] [Full Text]
Botelho, R. J., Hackam, D. J., Schreiber, A. D., Grinstein, S. (2000). Role of COPI in Phagosome Maturation. J. Biol. Chem. 275: 15717-15727 [Abstract] [Full Text]
Poon, P. P., Nothwehr, S. F., Singer, R. A., Johnston, G. C. (2001). The Gcs1 and Age2 ArfGAP proteins provide overlapping essential function for transport from the yeast trans-Golgi network. JCB 155: 1239-1250 [Abstract] [Full Text]
Sachse, M., Urbe, S., Oorschot, V., Strous, G. J., Klumperman, J. (2002). Bilayered Clathrin Coats on Endosomal Vacuoles Are Involved in Protein Sorting toward Lysosomes. Mol. Biol. Cell 13: 1313-1328 [Abstract] [Full Text]