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First published online June 8, 2005
doi: 10.1242/10.1242/dev.01886
Institute of Signaling, Developmental Biology and Cancer, UMR 6543 CNRS, University of Nice Sophia-Antipolis, Parc Valrose, 06108 Nice, cedex 2, France
* Author for correspondence (e-mail: noselli{at}unice.fr)
Accepted 29 April 2005
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SUMMARY |
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 TOP SUMMARY IntroductionMaterials and methodsResultsDiscussionREFERENCES |
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chains, Laminin A and
Perlecan. Capping of polar cells proceeds through a novel, basal-to-apical
transcytosis mechanism that involves the small GTPase Drab5. Apical capping is
transient and is followed by rapid shedding prior to the initiation of BC
migration, suggesting that the apical cap blocks migration. Consistently,
non-migratory polar cells remain capped. We further show that JAK/STAT
signalling and recruitment of outer BCs are required for correct shedding and
migration. The dynamics of the BM represents a marker of migratory BC,
revealing a novel developmentally regulated behaviour of BM coupled to
epithelial cell invasiveness.
Key words: Basement membrane, Border cells, Migration, JAK/STAT, Transcytosis, Collagen IV
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Introduction |
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TOPSUMMARYIntroductionMaterials and methodsResultsDiscussionREFERENCES |
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). Its selective synthesis and degradation is developmentally
regulated to favor cell rearrangements and migration. In cancer cells,
misregulation of ECM break-down strongly promotes cell invasion and metastasis
(Egeblad and Werb, 2002).
However, the behavior of the ECM in the early stages of migration, such as
during migratory cell selection and delamination from an epithelium, remains
poorly understood.
Drosophila border cells (BCs) represent an attractive genetic
model with which to study the invasiveness of epithelial cell clusters
(Montell, 2003;
Rorth, 2002). BCs are made of
two different cell types that appear sequentially during oogenesis, which form
a composite cluster delaminating from the anterior follicular epithelium to
migrate posteriorly into the egg chamber
(Fig. 1A). In early stages, a
pair of polar cells is determined at each pole of the egg chamber. Later, a
ring of six outer BCs, surrounding the anterior polar cells, are specified to
make a mature cluster, which, collectively with polar cells, is called the BC.
We, and others, have recently shown that the formation of the BC cluster
depends on signaling from polar cells to the outer BCs
(Beccari et al., 2002;
Ghiglione et al., 2002;
McGregor et al., 2002;
Silver and Montell, 2001). In
this process, polar cells express the secreted ligand Unpaired, activating the
JAK/STAT pathway in neighboring cells. Those cells receiving the highest
levels of the Unpaired ligand are committed into the outer BC fate and
participate in the formation of a migratory BC cluster.
Recent work has shown that BCs are guided during their migration towards
the oocyte through the EGFR and the PDGF/VEGF pathways
(Duchek and Rorth, 2001;
Duchek et al., 2001;
McDonald et al., 2003). Other
molecules are also essential for BC migration, including Slbo
(Montell et al., 1992),
ecdysone (a steroid hormone) (Bai et al.,
2000) and myosin VI
(Geisbrecht and Montell,
2002), as is the formation of long cellular actin-containing
extensions (Fulga and Rorth,
2002). However, the cellular events accompanying the initial
phases of BC formation and delamination are poorly understood, and it is
particularly unclear what are the role and behavior of the BM in this
process.
Here, we show that components of the BM undergo shuttling to the apical surface in anterior polar cells, through transcytosis involving Drab5 (Rab5 - FlyBase). This unusual apical capping is both asymmetrical and transient. Indeed, shortly before invasion starts, JAK/STAT signaling and interaction with outer BCs is required for shedding of the apical cap in polar cells, thus coordinating outer BC recruitment and invasiveness of the cluster. Strikingly, isolated polar cells that are unable to migrate maintain an apical cap.
The apical and transient targeting of BM materials in BCs may represent a novel marker of migratory cells during development and cancer, as well as a novel mechanism whereby the transition from pre-migratory to migratory phenotype is controlled.
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Materials and methods |
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TOPSUMMARYIntroductionMaterials and methodsResultsDiscussionREFERENCES |
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), and
658, 1700, 1973, 2840, 2867, G6 and G205
(Kelso et al., 2004), were
used to mark the basement membrane and the apical cap. GAL4-dependent
overexpression in the BC was performed using the slbo-GAL4,
vkgG454/CyO line crossed to UAS-X flies
(with X representing any reporter gene). The UAS lines used in this
study are listed in Table 1. To
overexpress eya, UAS-EYAB1 and UAS-EYAB2 were used (see FlyBase) (Bai
and Montell, 2002), and crossed to Upd-GAL4 (a gift from D. Montell). Clonal
analysis was performed using y w; vkgG454,
FRT40A/CyO crossed to either HS-Flp; HS-c-Myc,
FRT40A/CyO or UB-GFP, FRT40A/CyO; T155-GAL4, UAS-Flp/T155-GAL4,
UAS-Flp. Myc and nls-GFP were used as clonal markers.
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1 chain (Cg25C;
1:1000) were from J. Fessler (Blumberg et
al., 1988) and anti-GFP was a gift from R. Arkowitz (1:10,000).
Monoclonal antibodies against Crumbs (1:50), Armadillo (1:50), Fas2 (1D4;
1:50) and Fas3 (7G10; 1:50) were from the Developmental Studies Hybridoma
Bank; anti-Laminin A (1:3000) was a gift from S. Baumgartner
(Gutzeit et al., 1991),
anti-ß-galactosidase (1:1000) was from Promega and anti-c-Myc was from
Calbiochem (1:100). Secondary antibodies were anti-rabbit Alexa 488 (1:400) or
Texas Red (1:100), and anti-mouse Texas Red (1:100) or Alexa 488 (1:400), from
Molecular Probes.
Protein extracts were prepared from ovaries, loaded on SDS-PAGE gels and
blotted onto nitrocellulose filters. Type IV Collagen 1 and
2-GFP chains were detected using anti-1 and anti-GFP antibodies,
respectively.
Confocal microscopy and imaging
From one experiment to another, we found a small variation in the number of
egg chambers showing an apical cap in wild type (85±5%), probably
because of variations in the fixation conditions. To determine the percentage
of egg chambers showing an apical cap (Fig.
4G,H), wild-type and mutant egg chambers were stained and
processed at the same time. Thus, each experiment has its own control, which
is plotted in the histogram. At least three sets of experiments were performed
for each condition.
Images were taken using a Leica TCS-SP1 or a Zeiss LSM 510 Meta confocal microscope and processed using Photoshop 7.0 (Adobe). Three-dimensional reconstruction of anterior egg chambers and apical caps was made using Volocity 2.6 (Improvision).
Statistical analysis
The statistical analysis shown in Fig.
4G was made by comparing the means of the variables in each
experiment. Given the statistically high number of samples, we applied the
Bernoulli Rule. In each experiment, we tested the hypothesis that results are
equal versus the hypothesis that results are different (ShiK44A),
lower (Drab5S43N) or higher (Drab5WT) than the wild
type. We chose a confidence interval () and applied Student's
t-test to the data. The result of which indicates that the
probability that Drab5S43N is lower than wild type is 0.99 (99%),
the probability that ShiK44A and wild type are not different is
0.99 (99%), and the probability that Drab5WT is higher than wild
type is 0.85 (85%).
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Results |
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TOPSUMMARYIntroductionMaterials and methodsResultsDiscussionREFERENCES |
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2 chain [encoded by the viking (vkg) gene] fused to
GFP (Morin et al., 2001). The
resulting GFP-Vkg fusion protein is expressed under the control of the
endogenous vkg promoter and thus represents a faithful reporter of
Vkg expression. GFP-Vkg strongly accumulates basally in all egg chambers
(Fig. 1B; data not shown),
consistent with Collagen IV being a major component of the BM
(Fessler and Fessler, 1989).
Most surprisingly, we found that, in stage 8 egg chambers, GFP-Vkg also
accumulates apically into a discrete cap over the anterior polar cells
(Fig. 1B,C), but not over the
posterior ones (Fig. 1D). Only
anterior polar cells will recruit outer BCs and undergo migration
(Fig. 1A). Like GFP-Vkg,
antibodies against the Cg25C/Coll.IV 1 chain
(Fig. 1E-H) (Blumberg et al., 1988) and
Laminin A (Gutzeit et al.,
1991) mark the BM and co-localize with GFP-Vkg in the apical cap
(Fig. 1I-K). To determine
whether apical capping represents a general behavior of the BM, a series of
recently developed but uncharacterized protein-trap lines exhibiting BM
localization were analysed (Kelso et al.,
2004). Sequencing of these protein-trap lines identified a novel
GFP-Vkg fusion (G205; Fig. 1L;
see Fig. S1A in the supplementary material) and several insertions in the
perlecan/CG7981 gene (G6, 658, 1700, 1973, 2840, 2867;
Fig. 1M,N and Fig. S1B in the
supplementary material), which encodes a proteoglycan that is a major
component of BM. These results indicate that most, if not all, of the
components of the BM in stage 8 egg chambers form an apical cap over the
anterior polar cells.
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Apical capping is asymmetrical and dynamic
Three-dimensional imaging of anterior stage 8 egg chambers shows that the
apical cap is rod-shaped and runs along the apical surface
(Fig. 3A-F; see Movies 1 and 2
in the supplementary material). Interestingly, the apical cap preferentially
associates with one of the two polar cells (see below), thus revealing a
previously unknown intrinsic asymmetry within the pair of anterior polar
cells.
Careful staging of egg chambers indicates that apical capping is highly dynamic and proceeds through four discrete steps. (1) From stages 1-8 of oogenesis, GFP-Vkg and other BM component localization is restricted to the basal surface of epithelial cells (Fig. 3G and data not shown). (2) During stage 8, the formation of a discrete apical cap above each of the two polar cells is observed, suggesting that, initially, each polar cell makes its own apical cap (Fig. 3H, arrowheads; Fig. 2D,F). Subsequently, when the apical surface of polar cells constricts, one cap develops (large arrowhead) while the other remains rudimentary (small arrowhead), thus leading to asymmetrical capping (Fig. 3I-K). (3) The apical cap is kept in place at stages when polar cells undergo rounding and detach from the BM (Fig. 3J). In rare cases, it is possible to observe an intermediate stage showing two opposite caps, one at the basal and one at the apical surface (Fig. 3K). (4) Finally, when the BC cluster starts to migrate, the apical cap is no longer observed and only the basal cap remains (Fig. 3L). Thus, apical capping is transient, appearing at stage 8 and being shed at stage 9. The timing and cell-type specificity of apical capping indicate that BM cap dynamics are tightly coordinated with the formation of migratory border cells.
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).
Apical and adherens junction markers are reorganized during the transition
from an epithelial to a migratory phenotype, leading to an extension of the
apical and junctional domains and the adoption of a rosette-like shape
(Fig. 3M)
(Niewiadomska et al., 1999).
After migration, when BCs reach the oocyte and re-epithelialize, the apical
domain returns to its original organization
(Fig. 3O). Interestingly, we
found that polar cells keep a BM throughout the process, in a position
opposite to the apical side as shown by double staining with the apical marker
Crumbs (Fig. 3M,O). This is in
sharp contrast with outer BCs, whose BM is detached or degraded when they
delaminate from the follicular epithelium. This result indicates that contrary
to outer BCs, polar cells maintain a fully polarized phenotype with a normal
BM during migration.
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The above results suggest that the apical cap originates from outside the
polar cells. Transcytosis is a mechanism allowing proteins from one membrane
sub-domain to be targeted to another domain after internalization
(Tuma and Hubbard, 2003). To
test whether internalization could be a mechanism by which the apical cap
forms, we blocked Drab5 and Shibire (a Drosophila dynamin homolog)
function in the BCs. These proteins are required in intracellular trafficking
in Drosophila and other organisms
(Seto et al., 2002), and we
show here that both proteins are essential for BC migration
(Table 1;
Fig. 6). Interestingly, the
expression in BCs of a Drab5 dominant-negative (DN) form
(Drab5S43N) (Wucherpfennig et
al., 2003) results in the absence of the apical cap in stage 8 egg
chambers, as compared with wild type (Fig.
4D,E,G). Moreover, among clusters still showing a cap in
Drab5S43N egg chambers, 47% show a `micro-cap'
(Fig. 4F,H), which is twice as
frequent as in wild-type egg chambers (20%)
(Fig. 4H). Conversely, the
expression of Drab5WT induces a 5% increase in the number of egg
chambers with an apical cap (Fig.
4G). In this case, micro caps are less frequent (15%) than in wild
type (25%) (Fig. 4H).
The expression of a dominant-negative form of Shibire (ShiS44A)
(Moline et al., 1999) did not
block the formation of the apical cap (Fig.
4G). Thus, contrary to clathrin-dependent endocytosis, Drab5 and
Shi have distinct roles in the formation of an apical cap over anterior polar
cells.
We also tested the effect of other trafficking molecules and of signaling pathways known to be important for BC migration (see Table 1). None of these induced a defect in apical cap formation, indicating that Drab5 plays a specific role in this process.
Apical cap shedding requires JAK/STAT signaling and outer BCs
Once BC delaminate and start migration, the apical cap is no longer
observed, indicating that an active process is responsible for removing the BM
apically. It is thus important to determine the mechanism by which apical
shedding and migration are coordinated. One likely possibility is that outer
BCs themselves could control the status of the apical BM in polar cells. In
order to test this possibility, we blocked the formation of outer BCs by
expressing dominant-negative forms of Domeless (Dome) (Dome
Ext and
DomeCyt), the receptor of the JAK/STAT pathway. In wild-type egg
chambers, polar cells secrete the Unpaired ligand, which activates the
JAK/STAT pathway in neighboring cells and recruits them as outer BCs
(Fig. 1A) (Beccari et al., 2002;
Ghiglione et al., 2002;
McGregor et al., 2002;
Silver and Montell, 2001).
Those cells receiving the highest levels of Unpaired are committed into the
outer BC fate and participate in the formation of a migratory BC cluster.
Expression of dominant-negative forms of Dome lacking either the extracellular
or the intracellular receptor domain (DomeExt and DomeCyt,
respectively), induces most egg chambers to develop without outer BCs
(Ghiglione et al., 2002).
Consequently, the two polar cells remain at the anterior tip and do not
migrate (Fig. 7B). Strikingly,
the apical cap forms normally in DomeCyt stage 9 egg chambers but is
not shed in stage 10, or later, egg chambers
(Fig. 7A,B), suggesting that
outer BCs are required for removing of the apical cap. In order to confirm
this result, and to rule out the possibility that the absence of migration
itself could block shedding, migration of a fully formed BC cluster was
inhibited by expression of either a dominant-negative form of Drac
(DracN17) (Murphy and Montell,
1996) (Fig. 7C,D)
or a wild-type form of Dome (Ghiglione et
al., 2002) (Table
1). In both cases, and despite a lack of migration, the apical cap
forms normally and is shed like in wild-type clusters, confirming that outer
BCs are essential for shedding before the cluster starts migration, probably
by interacting back with the polar cells. Note that, in the Drac1 condition,
detachment from the BM appears normal, as indicated by the presence of a basal
cap (Fig. 7D), and the
migratory phenotype originates from actin cytoskeleton defects, as shown
previously (Geisbrecht and Montell,
2004; Murphy and Montell,
1996).
|
;
Llano et al., 2000). However,
we could not see any defect in apical cap dynamics upon expression of Dm1-MMP
(native or activated form) or the Drosophila MMP inhibitor DTIMP
(Timp - FlyBase; Table 1),
which suggests that a different protease or mechanism is responsible for
apical cap degradation. It is also important to mention that neither
Dynamin-dependent endocytosis (ShiK44A) nor lysosomal degradation (Drab7Q67L
and Dor) seem to be involved in cap formation or shedding (see
Table 1).
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Discussion |
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TOPSUMMARYIntroductionMaterials and methodsResultsDiscussionREFERENCES |
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). In
this case, migration is executed by migratory capable cells within the
cluster. Clusters illustrate how separate functions (tumorigenesis and
migration) can be merged through collaboration between two cell populations.
It is thus important to understand how migrating cell clusters are assembled
and organized. The BC cluster is made of two distinct populations of cells,
i.e. the polar cells and the outer BCs, making it a good model with which to
determine the cellular mechanisms underlying the recruitment and migration of
mixed cohorts of cells. Here, we identify three novel steps in the formation
of BCs (Fig. 7E). First, we
show that a developmentally regulated basal to apical transport of BM material
takes place in the polar cells, the first population of cells to form in the
cluster. The apical cap is the earliest known marker of anterior polar cells.
Second, the asymmetrical positioning of the apical cap suggests that despite
an apparent identity, the two polar cells are different and might play
distinct roles. Third, our data indicate that a two-way interaction takes
place between the two differentiated subpopulations of invasive cells before
they migrate. A first signal, activating the JAK/STAT pathway is sent by the
polar cells to recruit the outer BCs. In a second step, the outer BCs are
essential for shedding the apical cap of polar cells
(Fig. 7E).
Outer BCs are not required for apical cap formation
(Fig. 7A,B). Similarly, outer
BCs form normally in the absence of a cap
(Fig. 4; data not shown),
indicating that apical capping is not a pre-requisite for outer BCs to be
recruited and the cluster to be assembled. Interestingly, we found that
immotile polar cells remained capped (Fig.
7A,B). Thus, a possible role for apical capping is to block the
migration of immature clusters, a finding that could explain the long standing
observation that isolated polar cells cannot migrate on their own. Indeed, the
coordination between apical cap degradation and the recruitment of outer BCs
indicates that degradation of the apical cap could serve as a check point or
quality control ensuring that only finalized clusters can start migration. It
is important to note that degradation of the ECM at the leading edge of
migrating clusters is essential for tumour progression, and examples of cancer
cells showing a reduction or absence of some basement membrane markers,
including Collagen IV, have been reported. In particular, human
3/4 type IV Collagen is found at the apical surface in normal
colon tissue, but is absent in colorectal neoplastic cells
(Hiki et al., 2002), making
the differential distribution of type IV collagens potential diagnostic
markers for the invasiveness of cancer cells. The BC model will be central for
future studies aimed at understanding BM dynamics and function in invasive
clusters.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/132/13/3069/DC1
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 A. M. O'Reilly, H.-H. Lee, and M. A. Simon Integrins control the positioning and proliferation of follicle stem cells in the Drosophila ovary J. Cell Biol., August 25, 2008; 182(4): 801 - 815. [Abstract] [Full Text] [PDF]
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 O. Devergne, C. Ghiglione, and S. Noselli The endocytic control of JAK/STAT signalling in Drosophila J. Cell Sci., October 1, 2007; 120(19): 3457 - 3464. [Abstract] [Full Text] [PDF]
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A. Srivastava, J. C. Pastor-Pareja, T. Igaki, R. Pagliarini, and T. Xu Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion PNAS, February 20, 2007; 104(8): 2721 - 2726. [Abstract] [Full Text] [PDF]
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