ARTICLES
NATURE METHODS | VOL.9 NO.5 | MAY 2012 | 493
To dissect secretory traffic, we developed the retention
using selective hooks (RUSH) system. RUSH is a two-state
assay based on the reversible interaction of a hook protein
fused to core streptavidin and stably anchored in the donor
compartment with a reporter protein of interest fused to
streptavidin-binding peptide (SBP). Biotin addition causes a
synchronous release of the reporter from the hook. Using the
RUSH system, we analyzed different transport characteristics of
various Golgi and plasma membrane reporters at physiological
temperature in living cells. Using dual-color simultaneous
live-cell imaging of two cargos, we observed intra- and post-
Golgi segregation of cargo traffic, consistent with observation
in other systems. We show preliminarily that the RUSH system
is usable for automated screening. The system should help
increase the understanding of the mechanisms of trafficking
and enable screens for molecules that perturb pathological
protein transport.
It is now clear that there are many routes for proper transport,
modification and addressing of proteins in the secretory pathway
of cells. This had been anticipated because of the diversity of target
compartments (for example, plasma membrane, endosomes and
lysosomes) but also because of the existence of plasma membrane
subdomains
1–3
. Even for a simple transport route (such as the
endoplasmic reticulum (ER) to plasma membrane) in nonpolar-
ized cells, several independent pathways support the traffic of
different subsets of protein cargo
4–7
. A comprehensive view of
the mechanisms and dynamics of cargo sorting in these multiple
secretory pathways requires assays that allow the dissection of
the routes specific cargos follow. Ideally, these assays should be
adaptable to a large diversity of cargos, allow quantitative and
real-time trafficking observations and be amenable to large-scale
experiments. Such assays would enable more detailed study of the
large number of diverse trafficking regulators, such as families of
small GTPases or SNAP receptors, the majority of which remain
functionally unannotated.
Several approaches are currently used to image secretory traffic.
For instance, short-term reporter expression, either after DNA
microinjection or after photoconversion or photobleaching of a
Synchronization of secretory protein traffic in
populations of cells
Gaelle Boncompain
1,2
, Severine Divoux
1,2
, Nelly Gareil
1,2
, Helene de Forges
1,2
, Aurianne Lescure
3
,
Lynda Latreche
3
, Valentina Mercanti
1,2
, Florence Jollivet
1,2
, Graça Raposo
1,2
& Franck Perez
1–3
fraction of the target protein in single cells, has been used for this
purpose. These methods are frequently coupled with temperature
block and release to synchronize the reporter pool and allow traffic
through the secretory pathway to be followed quantitatively.
Temperature block (for example, 15 °C to block proteins in the ER
or 20 °C to block proteins in the Golgi
8,9
) has proven a powerful
tool for studying intracellular traffic, including in living cells, but
it also imposes a temporary arrest of virtually all biosynthetic
pathways in a mammalian cell. Another classical and powerful
method for cargo synchronization relies on a thermosensitive
viral glycoprotein (VSVGtsO45) that cannot exit from the ER at
the restrictive temperature of 39.5 °C (refs. 10,11). Synchronous
transport and processing at 32 °C can be monitored in living
cells
12–14
. However, the restrictive and permissive temperatures
for this system are not fully physiological and complicate the use of
this system for systematic screening. In addition, the VSVGtsO45
system cannot be easily adapted to the analysis of a large diversity
of cargos. An alternative method
15
relies on the fusion of the pro-
tein of interest with conditional aggregation domains, resulting
in the aggregation of the fusion protein in the ER. This aggrega-
tion is reversed by the addition of a small ligand, allowing syn-
chronous and controlled secretion of soluble or transmembrane
proteins
15–18
. However, this approach is not applicable to proteins
that cannot be tagged on their luminal domains and cannot be used
for synchronization after the ER. A regulated trafficking system
has also been developed that depends on the induction of reporter
expression in Drosophila melanogaster cells
19
. It has been used for
screening
20,21
but because of slow kinetics would be less adapted to
real-time analysis of early trafficking steps (such as ER export).
Thus there is still an unmet need for a versatile trafficking
assay that allows efficient synchronization of diverse cargo, under
physiological conditions, permits quantitative live cell imaging
and is amenable to automated screening. Here we describe such
a system, named RUSH, which relies on the selective retention
and release of cargo molecules from a donor compartment.
We showed that the RUSH system can be used to study and quan-
tify the trafficking of diverse proteins in live cells or in end-point
assays, and that it shows potential for automated quantitative
imaging and screening in the future.
1
Institut Curie, Centre de Recherche, Paris, France.
2
Centre National de la Recherche Scientifique, Unité Mixte de Recherche 144, Paris, France.
3
The BioPhenics
Laboratory, Institut Curie, Paris, France. Correspondence should be addressed to F.P. (franck.perez@curie.fr).
RECEIVED 2 AUGUST 2011; ACCEPTED 24 JANUARY 2012; PUBLISHED ONLINE 11 MARCH 2012; DOI:10.1038/NMETH.1928
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