NATURE STRUCTURAL & MOLECULAR BIOLOGY VOLUME 12 NUMBER 2 FEBRUARY 2005 107
and that these interactions are sufficient to
form a complex via binding to Sar1p without
Sec24p-Bet1p interactions. Hence, the FRET
assay was sensitive enough to dissect specific
interactions among coat components in the
COPII complex.
Sato and Nakano
3
then used the FRET assay
to examine whether the complex of Sec24/23p
bound to cargo (SNARE in this study) remains
associated with the membrane after Sar1p-GTP
is hydrolyzed (Fig. 1a). When YFP-Sec24/23p
was added to CFP-Bet1p-SNARE liposomes
preloaded with Sar1p-GTP, an initial increase
in FRET signal (comparable to that of GMP-
PNP) was observed, indicative of Sar1p-
mediated formation of a complex between
YFP-Sec24/23p and CFP-Bet1p-SNARE. Soon
thereafter, the FRET signal declined owing to
disassembly of the complex upon Sar1p-GTP
hydrolysis. Because the decline was slower than
for Sar1p-GTP hydrolysis (monitored by tryp-
tophan fluorescence) the results indicate that
the complex of Sec24p and Bet1p-SNARE is
stable on membranes for a short period after
hydrolysis of Sar1p-GTP. This behavior of
COPII coat components is reminiscent of that
of COPI components, which remain associated
with Golgi membranes after Arf1-GTP hydro-
lysis (determined from photobleaching studies
in living cells)
8
. Therefore, there seems to be
a commonality in the mechanism(s) whereby
coat components assemble into metastable
coats on the membrane.
To determine whether the persistent associa-
tion of Sec24/23p with membranes after Sar1p-
GTP hydrolysis results from Sec24p interacting
specifically with Bet1p-SNARE, the authors
repeated the FRET assay using the mutant
Bet1p-SNARE, which lacks the Sec24p-binding
sequence. In this case, the signal declined at the
same rate as Sar1p-GTP hydrolysis. Hence, the
delay in membrane dissociation of Sec24/23p
after Sar1-GTP hydrolysis requires a specific
interaction between SNARE-cargo and Sec24p.
This finding raises the possibility that SNAREs
serve as scaffolds for Sar1p on the ER, directing
Sec24/23p GAP activity toward Sar1p.
In the last set of experiments, the authors
examined the behavior of YFP-Sec24/23p and
CFP-Bet1p-SNARE on membranes under
conditions of multiple rounds of Sar1p-GTP
hydrolysis (Fig. 1b). Here, the reaction mix was
supplemented with Sec12p, which catalyzes
efficient GDP-GTP exchange at Sar1p. Notably,
the FRET signal persisted through the exchange
reaction, indicating that YFP-Sec24/23p asso-
ciation with Bet1p-SNARE is maintained, most
likely because Sec12p continuously reactivates
Sar1p to its GTP-bound form. This finding is
important as it explains how kinetically stable
COPII complexes can potentially form during
Sar1p-GTPase cycles. In this scenario, the con-
tinuous interaction of Sec24/23p with cargoes
on the membrane—owing to repeated cycles of
Sar1p-GTP hydrolysis and reactivation—leads
to the formation of ‘coated’ domains or buds
that are metastable; that is, they exist as long
as Sar1p-GTP is being supplied to the domain.
Because Sec12p is strictly localized to ER mem-
branes, when the coated domains pinch off of
the membrane, their coat is rapidly shed owing
to depletion of Sar1p-GTP in the absence of
GDP-GTP exchange activity. Not all interactions
between different types of cargo and Sec24/23p
may be stabilized sufficiently on the membrane
during Sar1p-GTPase cycles to produce such
coated domains. The authors thus speculate that
oligomerization of cargo proteins may create
combined signals for high-affinity binding to
Sec24/23p. This would lead to the formation of
cargo oligomer–Sec24/23p complexes, which in
the presence of continuous Sar1p-GTPase cycles
would create ‘coated’ sorting domains contain-
ing more diverse types of cargo
9
.
Many other aspects of COPII coat assembly
and its modulation by cargo could potentially
be studied using the FRET-based approach
of Sato and Nakano
3
. For example, how does
Sec13/31p interact with Sec23/24p to crosslink
adjacent Sec23/24p complexes into a structural
scaffold? Does Sec13/31p play a role in accel-
erating Sec23p-mediated GAP activity? As
the FRET-based assay can be used to dissect
recruitment and cargo-capture events during
the assembly of other coat systems on mem-
branes, including COPI and clathrin coats, this
assay offers a general new approach for clari-
fying protein-protein interactions and their
kinetics on the membrane.
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ACEing GPI release
Satyajit Mayor
A recent study shows that the testicular angiotensin converting enzyme (ACE) has a new unexpected activity: it is
responsible for cleaving GPI off from proteins anchored on the sperm cell membrane.
Fertilization is the process by which a sperm
and an egg unite to form the first cell in the
development of a multicellular organism. In
mammals, the membrane properties of a viable
and motile sperm undergo drastic alterations
during the encounter with the mature oocyte,
leading to binding and eventually the fusion
with the mature oocyte (for a recent review
on the fertilization process, see ref. 1). Many
glycosylphosphatidylinositol (GPI)-anchored
proteins, such as CD52, PH20 and TESP2, in
the sperm are involved in triggering the matu-
ration of the sperm and in oocyte recognition
events. Most of these proteins are released in the
medium surrounding the sperm, some during
epididymal maturation, and others after a spe-
cific membrane altering process termed ‘sperm
capacitation’ (Fig. 1), in which a drastic reorga-
nization of the membrane of the sperm takes
place, partially due to efflux of β-hydroxysterols
(cholesterol in mammals). This culminates in
the initiation of the acrosome reaction
2
.
Kondoh et al.
3
reported, in a recent issue of
Nature Medicine, that testicular ACE specifi-
cally cleaves GPI-anchored proteins from the
membrane tether. This observation unites three
seemingly disparate facets of the fertilization
process: (i) the requirement for GPI-anchored
sperm membrane proteins, (ii) a specific
requirement for ACE in germ cells and (iii) a
role for cholesterol removal. Furthermore, their
The author is in the Cellular Organization and
Signaling Group, National Centre for Biological
Sciences, Bellary Road, Bangalore 560 065, India.
e-mail: mayor@ncbs.res.in
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