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Vol. 9, Issue 6, 1323-1337, June 1998
Division of Hematology, Department of Internal Medicine, Washington
University School of Medicine, St. Louis, Missouri 63110
Association of the Golgi-specific adaptor protein complex 1 (AP-1)
with the membrane is a prerequisite for clathrin coat assembly on the
trans-Golgi network (TGN). The AP-1 adaptor is efficiently recruited
from cytosol onto the TGN by myristoylated ADP-ribosylation factor 1 (ARF1) in the presence of the poorly hydrolyzable GTP analog guanosine
5'-O-(3-thiotriphosphate) (GTP
S). Substituting GTP
for GTPS, however, results in only poor AP-1 binding. Here we show
that both AP-1 and clathrin can be recruited efficiently onto the TGN
in the presence of GTP when cytosol is supplemented with ARF1. Optimal
recruitment occurs at 4 µM ARF1 and with 1 mM GTP. The AP-1 recruited
by ARF1·GTP is released from the Golgi membrane by treatment with 1 M
Tris-HCl (pH 7) or upon reincubation at 37°C, whereas AP-1 recruited
with GTPS or by a constitutively active point mutant, ARF1(Q71L),
remains membrane bound after either treatment. An incubation performed
with added ARF1, GTP, and AlFn, used to block ARF
GTPase-activating protein activity, results in membrane-associated
AP-1, which is largely insensitive to Tris extraction. Thus, ARF1·GTP
hydrolysis results in lower-affinity binding of AP-1 to the TGN. Using
two-stage assays in which ARF1·GTP first primes the Golgi membrane at
37°C, followed by AP-1 binding on ice, we find that the high-affinity
nucleating sites generated in the priming stage are rapidly lost. In
addition, the AP-1 bound to primed Golgi membranes during a
second-stage incubation on ice is fully sensitive to Tris extraction,
indicating that the priming stage has passed the ARF1·GTP hydrolysis
point. Thus, hydrolysis of ARF1·GTP at the priming sites can occur
even before AP-1 binding. Our finding that purified clathrin-coated
vesicles contain little ARF1 supports the concept that ARF1 functions
in the coat assembly process rather than during the vesicle-uncoating step. We conclude that ARF1 is a limiting factor in the GTP-stimulated recruitment of AP-1 in vitro and that it appears to function in a
stoichiometric manner to generate high-affinity AP-1 binding sites that
have a relatively short half-life.
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