Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments

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Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments

PJ Peters, VW Hsu, CE Ooi, D Finazzi, SB Teal, V Oorschot, JG Donaldson and RD Klausner
Cell Biology and Metabolism Branch, NICHD, National Institutes of Health, Bethesda, Maryland 20892.

The ARF GTP binding proteins are believed to function as regulators of membrane traffic in the secretory pathway. While the ARF1 protein has been shown in vitro to mediate the membrane interaction of the cytosolic coat proteins coatomer (COP1) and gamma-adaptin with the Golgi complex, the functions of the other ARF proteins have not been defined. Here, we show by transient transfection with epitope-tagged ARFs, that whereas ARF1 is localized to the Golgi complex and can be shown to affect predictably the assembly of COP1 and gamma-adaptin with Golgi membranes in cells, ARF6 is localized to the endosomal/plasma membrane system and has no effect on these Golgi-associated coat proteins. By immuno-electron microscopy, the wild-type ARF6 protein is observed along the plasma membrane and associated with endosomes, and overexpression of ARF6 does not appear to alter the morphology of the peripheral membrane system. In contrast, overexpression of ARF6 mutants predicted either to hydrolyze or bind GTP poorly shifts the distribution of ARF6 and affects the structure of the endocytic pathway. The GTP hydrolysis-defective mutant is localized to the plasma membrane and its overexpression results in a profound induction of extensive plasma membrane vaginations and a depletion of endosomes. Conversely, the GTP binding-defective ARF6 mutant is present exclusively in endosomal structures, and its overexpression results in a massive accumulation of coated endocytic structures.
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Moss, J., Vaughan, M. (1998). Molecules in the ARF Orbit. J. Biol. Chem. 273: 21431-21434 [Full Text]
Franco, M., Boretto, J., Robineau, S., Monier, S., Goud, B., Chardin, P., Chavrier, P. (1998). ARNO3, a Sec7-domain guanine nucleotide exchange factor for ADP ribosylation factor 1,�is involved in the control of Golgi structure and function. Proc. Natl. Acad. Sci. USA 95: 9926-9931 [Abstract] [Full Text]
Zhang, Q., Cox, D., Tseng, C.-C., Donaldson, J. G., Greenberg, S. (1998). A Requirement for ARF6 in Fcgamma Receptor-mediated Phagocytosis in Macrophages. J. Biol. Chem. 273: 19977-19981 [Abstract] [Full Text]
Ooi, C. E., Dell'Angelica, E. C., Bonifacino, J. S. (1998). ADP-Ribosylation Factor 1 (ARF1) Regulates Recruitment of the AP-3 Adaptor Complex to Membranes. JCB 142: 391-402 [Abstract] [Full Text]
Sata, M., Donaldson, J. G., Moss, J., Vaughan, M. (1998). Brefeldin A-inhibited guanine nucleotide-exchange activity of Sec7 domain from yeast Sec7 with yeast and mammalian ADP ribosylation factors. Proc. Natl. Acad. Sci. USA 95: 4204-4208 [Abstract] [Full Text]
Haft, C. R., de La Luz Sierra, M., Hamer, I., Carpentier, J.-L., Taylor, S. I. (1998). Analysis of the Juxtamembrane Dileucine Motif in the Insulin Receptor. Endocrinology 139: 1618-1629 [Abstract] [Full Text]
Yang, C. Z., Heimberg, H., D'Souza-Schorey, C., Mueckler, M. M., Stahl, P. D. (1998). Subcellular Distribution and Differential Expression of Endogenous ADP-ribosylation Factor 6�in Mammalian Cells. J. Biol. Chem. 273: 4006-4011 [Abstract] [Full Text]
D'Souza-Schorey, C., van Donselaar, E., Hsu, V. W., Yang, C., Stahl, P. D., Peters, P. J. (1998). ARF6 Targets Recycling Vesicles to the Plasma Membrane: Insights from an Ultrastructural Investigation. JCB 140: 603-616 [Abstract] [Full Text]
Caumont, A.-S., Galas, M.-C., Vitale, N., Aunis, D., Bader, M.-F. (1998). Regulated Exocytosis in Chromaffin Cells. TRANSLOCATION OF ARF6 STIMULATES A PLASMA MEMBRANE-ASSOCIATED PHOSPHOLIPASE D. J. Biol. Chem. 273: 1373-1379 [Abstract] [Full Text]
Monier, S, Chardin, P, Robineau, S, Goud, B (1998). Overexpression of the ARF1 exchange factor ARNO inhibits the early secretory pathway and causes the disassembly of the Golgi complex. J. Cell Sci. 111: 3427-3436 [Abstract]