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First published online 25 July 2007
doi: 10.1242/dev.010447
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Centre for Developmental and Biomedical Genetics, Department of Biomedical Science, University of Sheffield, Western Bank, Sheffield S10 2TN, UK.
Author for correspondence (e-mail:
d.strutt{at}sheffield.ac.uk)
Accepted 20 June 2007
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SUMMARY |
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 TOP SUMMARY INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key words: Cell migration, Frizzled, Planar polarity, Strabismus, Drosophila
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INTRODUCTION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). In single-cell
migration, junctional contacts are lost, although cells might still remain
loosely associated in small groups or chains. Because this can be easily
studied in cultured cells, it is relatively well-characterised. During
collective cell migration, junctional contacts are maintained between groups
of moving cells. Such coordinated movement of cell groups is a key event in
organogenesis and has been implicated in disease states such as cancer
metastasis (Friedl et al.,
2004; Lecaudey and Gilmour,
2006). Well-studied examples of collective cell migration include
the movement of relatively small groups of cells, such as border cell
migration during Drosophila oogenesis
(Montell, 2003) and movement
of the lateral line primordium in fish and amphibians
(Ghysen and Dambly-Chaudière,
2004), as well as the rearrangement of sheets of cells such as
that which occurs during Drosophila dorsal closure
(Jacinto et al., 2002) and
vertebrate gastrulation (Keller,
2002). A key feature of collective cell migration is that it
permits the coordinated movement of both motile and non-motile cells together
in a single group. However, because collective cell migration can only be
studied in the context of developing organisms, it remains poorly
understood.
In recent years, a great deal of progress has been made in understanding
how cell polarity is coordinated in developing tissues. In many contexts in
both Drosophila and vertebrates, a conserved planar polarity pathway
mediates local cell-cell interactions to ensure that neighbouring cells adopt
the appropriate polarity (Strutt,
2003; Veeman et al.,
2003; Klein and Mlodzik,
2005). Central to this is a core group of polarity proteins, which
includes the seven-pass transmembrane receptor Frizzled (Fz), the four-pass
transmembrane protein Strabismus (Stbm, also known as Van Gogh) and the
cytoplasmic proteins Dishevelled (Dsh) and Prickle (Pk). This core is involved
in diverse patterning events, from bristle and hair polarity on the body
surface of flies to convergent extension and neural crest migration in
vertebrate embryos (Strutt,
2003; Wallingford et al.,
2002; De Calisto et al.,
2005).
Given the requirement for planar polarity pathway function for efficient
convergent extension movements, it is a good candidate to coordinate the
collective migration of cells in other contexts. Therefore, we examined its
requirement in border cell migration in the Drosophila egg chamber,
which represents a particularly well-characterised and genetically tractable
model of collective cell migration. The early egg chamber consists of an
oocyte and nurse cells, of germline origin, surrounded by a single layer of
follicular epithelium of somatic origin
(Fig. 1A, stage 8). At each end
of this epithelium is a pair of differentiated cells known as the polar
follicle cells (Ruohola et al.,
1991). During egg chamber maturation, the outer follicle cells
undergo a series of stereotypic cell movements
(Fig. 1A, stage 9). The
anterior polar follicle cells signal to their neighbours, inducing a partial
epithelial-to-mesenchymal transition
(Silver and Montell, 2001).
These neighbouring cells, known as the border cells, delaminate from the
epithelium, invade between the nurse cells and migrate to the anterior border
of the oocyte, carrying the polar follicle cells along with them.
Concurrently, the outer follicle cells also rearrange such that they all come
into contact with the oocyte (Fig.
1A, stage 10) (Montell,
2003).
The direction of border cell migration is determined by gradients of
ligands for receptor tyrosine kinases, produced in the oocyte
(Duchek and Rørth, 2001;
Duchek et al., 2001). Within
the migrating cluster, the border cells remain attached to one another and to
the polar follicle cells by stable epithelial junctions
(Niewiadomska et al., 1999).
The region of the border cells that is linked neither to the polar follicle
cells nor to each other appears to be mesenchymal and is motile.
Here, we show that planar polarity gene function is required for efficient border cell migration. Our results support a model in which the planar polarity pathway is required both in the polar follicle cells and the border cells, promoting the production of actin-rich protrusions during migration.
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MATERIALS AND METHODS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Mutant
follicle cell clones were induced using the FLP/FRT system
(Xu and Rubin, 1993):
1-3-day-old females of genotypes hs-FLP; FRT42 stbm6/FRT42
arm-lacZ or hs-FLP; fz15 FRT80/arm-lacZ FRT80 were
heat-shocked for 1 hour twice daily at 37°C for 3 days, then dissected 3-6
days after the last heat shock. Border cell migration experiments were scored blind. For wholly mutant egg chambers, all alleles tested (except for the slbo and Wnt4 controls) were crossed out for 10-20 generations to w1118, to provide a common genetic background, and w1118 was used as the control. For GAL4/UAS overexpression and RNAi-knockdown experiments, the controls were siblings lacking the UAS insert or the GAL4 driver, both these controls being significantly different from the experimental samples but not from each other. To test for defects caused by insertion of the RNAi transgenes, lines containing only the slbo-lacZ marker and the insertion were also scored (data not shown). Significance was scored between an experimental line and its control using the significance test for a difference in two proportions (Statistics at Square One, www.bmj.com). The mosaic data was analysed using Chi-squared tests, incorporating the Yates' correction for small sample sizes. Expected values were calculated by counting the frequency of wild-type to mutant cells in each cluster and calculating the probability of a leading cell being wild-type due to random assortment.
To quantitate the actin protrusions in border cell clusters, egg chambers from control and mutant flies were dissected in a single experiment and processed in parallel. Confocal z-stacks were captured throughout the entire depth of representative clusters for each genotype and the total number of actin protrusions was then counted for eight clusters selected at random. There was no statistically significant difference between the numbers of protrusions observed between different mutant genotypes (fz21, stbm6 and dsh1), whereas each mutant genotype showed a highly significant difference from the control w1118 chambers (P<10-7, t-test). As with the border cell migration experiments, the mutant alleles had previously been crossed out to the w1118 control stock for 10-20 generations to provide a common genetic background. Mutant chambers were additionally compared to control chambers processed in parallel in at least two independent experiments and, in each case, more protrusions were observed in the control chambers than in the mutant chambers.
Levels of GFP-RhoA in the cytoplasm versus the membranes of border cells were quantitated from confocal XY sections through border cell clusters, using NIH Image. The average level of GFP-RhoA fluorescence in the border cell cytoplasm was compared to the peak levels of GFP-RhoA fluorescence in the border cell membrane.
Molecular biology
RNAi constructs were made in the pWIZ vector
(Lee and Carthew, 2003)
against the first exon of fz (bp 682-1332, Accession: AY051808), the
second exon of stbm (bp 413-1312, Accession: AF044208) and a 1000 bp
segment within dsh (bp 705-1728, Accession: AF044208). Sequence
analysis showed no off-target matches of more than 17 bp for the fz
construct, 18 bp for the stbm construct and a single off-target match
of 20 bp for the dsh construct. The RNAi lines gave the expected
loss-of-function phenotypes in the wing, eye and notum, accompanied by loss of
Fz/Dsh/Stbm immunolabelling as appropriate. As an additional control for
specificity, the fz and stbm RNAi phenotypes were also found
to be enhanced in backgrounds heterozygous for fz and stbm
gene function, respectively. To make Actin-EGFP-RhoA, the
RhoA ORF was tagged at the N-terminus with EGFP and inserted
downstream of the Actin5C promoter in pCasper4. This construct
recapitulates known RhoA localisation patterns
(Magie et al., 2002).
Histology
Ovaries were generally dissected, fixed and antibody/X-gal stained as
described (Verheyen and Cooley,
1994). To preserve the actin cytoskeleton, egg chambers were
dissected and fixed as previously described
(Frydman and Spradling, 2001),
except that Schneider's medium was used in place of Grace's.
Primary antibodies used were 1:4000 rabbit anti-ß-galactosidase
(Cappel), 1:100 mouse anti-Armadillo-N2 7A1 (DSHB), 1:400 rabbit
anti-Strabismus (Rawls and Wolff,
2003), 1:50 mouse anti-Rho-p1D9 (DSHB)
(Magie et al., 2002), 1:1000
rabbit anti-Stat92E (Chen et al.,
2003) and 1:10 rat anti-DE-Cad2
(Oda et al., 1994). Rabbit
antibodies against Fz were raised using a His-tagged fusion protein containing
residues 40-252, and affinity purified using a GST-tagged fusion protein
containing residues 40-240. Secondary antibodies used were
anti-rabbit-Alexa-Fluor-568, anti-rabbit-Alexa-Fluor-488 and
anti-mouse-Alexa-Fluor-488 at 1:1000 (Molecular Probes), and anti-rat-Cy2 and
anti-mouse-Cy5 at 1:400 (Jackson). Actin was visualised with phalloidin-Texas
Red and phalloidin-FITC at 1:200 (Molecular Probes). Fluorescent images were
captured on a Leica SP confocal and processed using NIH Image and Adobe
Photoshop.
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RESULTS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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To address whether core planar polarity gene function is required
specifically in the border cell cluster, we used RNAi-mediated knockdown of
gene function, coupled with tissue-specific expression under the control of
the GAL4/UAS system (Brand and Perrimon,
1993). The slbo-GAL4 driver expresses specifically in the
border cells upon initiation of migration (dark green cells in
Fig. 1A)
(Rørth et al., 1998).
Knockdown of fz, stbm or dsh transcripts using this driver
results in a significant delay in border cell-cluster migration, relative to
the concomitant movement of the outer follicle cells over the egg chamber
surface (Fig. 1B). This
suggests that planar polarity gene function is required in the border cells
for cluster migration to occur efficiently. Two aspects of the phenotype are
particularly noteworthy: first, most border cells eventually reach the oocyte
(not shown but see Fig. S1B in the supplementary material); second, we never
observed any guidance defects, such as border cell clusters failing to migrate
in the correct direction. Hence, we conclude that the previously identified
RTK-mediated guidance cues (Duchek and
Rørth, 2001; Duchek et
al., 2001) are intact, but that the ability of the border cell
cluster to efficiently migrate in response to these cues is impaired.
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; Strutt et al.,
1997). Consistent with this, we found that overexpressing either
fz or stbm in the border cells results in delayed migration
(Fig. 1C). This suggests that
the planar polarity pathway functions in a similar manner in border cells as
in other tissues. Taken together, the observed delays in border cell migration following three independent methods of altering core planar polarity gene function (i.e. classical loss-of-function mutations, transcript knockdown by RNAi and overexpression of the gene products), for two independent core polarity genes (fz and stbm), provides strong evidence that the planar polarity pathway is required in border cells for efficient migration.
To further characterise planar polarity gene function in border cells, we
used mitotic recombination to generate genetically mosaic clusters. Border
cells, polar follicle cells and the nurse cells through which the cluster
migrates are derived from different cell lineages
(Margolis and Spradling,
1995); therefore, it is possible to generate clusters in which a
subset of the migratory border cells lack gene function, but the non-migratory
polar follicle cells and the substrate nurse cells retain function. It has
recently been demonstrated that the relative position of an individual border
cell within the migrating cluster is very fluid, with an individual cell
potentially able to occupy leading, lateral and lagging roles during migration
(Prasad and Montell, 2007).
Furthermore, earlier studies have shown that, if cells within a cluster lack
activity of a gene that is required for proper motility, then these cells will
partition to the lagging (anterior) edge of the cluster, whereas cells that
retain gene function are found at the leading (posterior) edge
(Niewiadomska et al., 1999;
Rørth et al., 2000). We
examined clusters in which either fz or stbm activity was
removed from a subset of border cells. In both cases, mutant border cells were
predominantly found at the lagging edge of the clusters, whereas cells that
retained gene function showed a strong preference to migrate at the leading
edge (Fig. 1D). This confirms
that the planar polarity pathway promotes border cell motility, and,
furthermore, demonstrates that pathway function is required autonomously in
the border cells themselves.
Planar polarity pathway function is not required for normal slow border cells, DE-Cadherin or Stat92E expression
The planar polarity pathway has been implicated in the regulation of both
gene expression and cell fate, as well as in the modulation of the
cytoskeleton (Strutt, 2003).
To investigate how planar polarity signalling promotes border cell migration,
we examined the expression of factors previously shown to be important for
border cell fate and motility.
The transcription factor encoded by the slow border cells
(slbo) gene (Montell et al.,
1992; Rørth et al.,
2000) and the cell adhesion molecule DE-Cadherin (DE-Cad, also
known as Shotgun-FlyBase) (Niewiadomska et
al., 1999) are both required for efficient migration of individual
border cells. Therefore, it is possible that the planar polarity pathway could
regulate the levels of these proteins. However, in egg chambers wholly lacking
planar polarity gene function, slbo expression
(Fig. 2A-D), and DE-Cad
expression and subcellular distribution
(Fig. 2E-H) appear normal.
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; Silver et al.,
2005), and the JAK/STAT pathway has been previously implicated in
planar polarity signalling (Zeidler et
al., 1999). However, we found that Stat92E expression and nuclear
localisation was also normal in border cell clusters lacking fz and
stbm function (Fig.
2I-K). Thus, judging from these examples, border cell fate and
gene expression is normal in these mutants.
Border cells with altered planar polarity pathway function have abnormal actin protrusions
By contrast, examination of the actin cytoskeleton of border cells from
mutant egg chambers did reveal significant defects. Wild-type border cells
showed prominent actin-rich protrusions
(Fig. 3A). Removal of fz,
stbm or dsh activity resulted in the loss of prominent
protrusions and a more even actin distribution over the border cell surface
(Fig. 3B-D). Whereas border
cell clusters from the control w1118 stock showed an
average of 94.8 protrusions per cluster (n=8), clusters in an
fz21 background showed an average of 38.4 protrusions
(n=8), stbm6 showed 37.0 (n=8) and
dsh1 showed 42.4 (n=8). We observed no clear
directional bias, suggesting that the planar polarity pathway affects the
frequency but not the orientation of such actin-rich protrusions. However,
given the complex morphology of the border cell cluster, an effect on
protrusion orientation cannot be ruled out.
A similar phenotype was observed upon knockdown of fz transcripts specifically in border cells (Fig. 3E). Furthermore, overexpression of fz and stbm in border cells also disrupted the production of large actin protrusions (Fig. 3F,G), suggesting that precise levels or spatial distribution of pathway activity is important for the correct production of stable actin structures. These results support the view that the motility defects observed in border cells with altered planar polarity pathway function are due to abnormal cytoskeletal dynamics.
RhoA GTPase function is required for border cell migration and is regulated by the planar polarity pathway
In the Drosophila wing and eye, the planar polarity pathway
positively regulates the activity of the cytoskeleton modulator RhoA GTPase.
Loss of RhoA function leads to defects in both the rotation of ommatidial
clusters in the eye and the production of actin-rich trichomes in the wing
(Strutt et al., 1997). Thus,
RhoA is a good candidate for mediating the effects of the planar polarity
pathway in border cells.
We examined the effects of the inactivation and activation of RhoA in
migrating border cells. We found that expression of a dominant-negative form
of RhoA led to the normally compact border cell cluster becoming spread out
along the anteroposterior axis, with the trailing edges of cells failing to
retract towards the cell bodies (Fig.
3H). This is consistent with studies in other migrating cells in
which RhoA is required for retraction of the trailing edge
(Raftopoulou and Hall, 2004).
Overall, border cell migration is strongly delayed and, in any particular
cluster, many cells never reach the oocyte. By contrast, expression of a
constitutively active RhoA produced clusters in which the border cells were
tightly rounded with no large actin protrusions, indicative of excessive
retractive activity (Fig. 3K).
This also delayed migration, although less severely than expression of
dominant-negative RhoA, with approximately 50% of clusters showing an overall
delay relative to controls. Consistent with its positive role on RhoA activity
in other tissues (Strutt et al.,
1997), reduction of planar polarity pathway function was able to
ameliorate the effects of RhoA activation, leading to less-rounded cells
showing obvious actin protrusions (Fig.
3L), but did not alter the effects of RhoA inactivation
(Fig. 3I).
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Core planar polarity gene function is additionally required in the non-migratory polar follicle cells
Border cell migration depends not only on the motile border cells, but also
on the presence of the non-migratory polar follicle cells in the cluster;
these cells form adherens junctions with the border cells and signal to them
(Niewiadomska et al., 1999;
Han et al., 2000;
Silver and Montell, 2001). We
investigated whether border cell migration also requires planar polarity gene
function in the polar follicle cells by using RNAi-mediated knockdown of
transcripts specifically in these cells. Knockdown of either fz or
stbm resulted in delayed border cell migration, but no delay was
observed upon knockdown of dsh
(Fig. 4A). Recent work in the
Drosophila wing has shown that dsh is not required for
intercellular communication mediated by the planar polarity pathway, but is
necessary to couple such signals to downstream effectors
(Strutt and Strutt, 2007).
These results suggest that Fz/Stbm-dependent cell-cell communication in the
polar follicle cells is required for efficient border cell migration, but that
downstream pathway effectors are not required in these non-migratory
cells.
To verify the specificity of the requirement for fz and
stbm in the polar follicle cells, we again examined genetically
mosaic border cell clusters. We obtained border cell clusters in which both
polar follicle cells lacked either fz or stbm function, but
in which some of the border cells retained activity. The number of such
clusters was small, because loss-of-function clones are rarer in the polar
follicle cell lineage than in the border cell lineage
(Margolis and Spradling,
1995). Contrary to what was observed in mosaic clusters in which
both polar cells retained fz or stbm activity, in clusters
in which both polar follicle cells lacked activity, we no longer observed a
preference for non-mutant border cells to partition to the leading edge of the
cluster (Fig. 4B). From this we
deduce that planar polarity pathway function only confers a migratory
advantage on border cells if the polar follicle cells also have fz
and stbm function. Therefore, a Fz/Stbm-dependent signal must pass
from the polar cells, either directly or indirectly, to the border cells, and
this signal is required in the border cells for planar polarity pathway
function to enhance their migration.
These results indicate a requirement for fz and stbm in the polar follicle cells, but do not address whether the requirement is in one or both cells, or whether it requires direct contact between polar follicle cells and responding border cells. Therefore, we examined the positions of wild-type and mutant cells within mosaic clusters in which only one polar cell retained fz or stbm activity.
In such mosaic clusters lacking fz activity in one polar follicle cell, we made an important observation (Fig. 4C): the polar cell that retained fz function was always positioned towards the leading edge of the cluster, contacting the leading border cells, whereas the fz mutant polar cell was always positioned towards the lagging end of the cluster, contacting the lagging border cells. This result was independent of the genotype of the border cells. Consequently, border cells are positioned within the cluster according to the genotype of the polar cell with which they make junctional contact. Thus, we conclude that the motility of either wild-type or fz mutant border cells is enhanced by contact with a fz-expressing polar cell.
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We can summarise our findings from the mosaic analysis data as follows: in clusters that retain fz and stbm activity in the non-migratory polar follicle cells, border cell motility is cell-autonomously enhanced by fz and stbm function; second, this enhancement of border cell motility by planar polarity pathway function requires direct contact with a fz-expressing polar follicle cell; and third, this enhancement also requires stbm activity in at least one polar follicle cell, but this cell does not need to directly contact a border cell to enhance its migration.
Fz and Stbm proteins are localised within migrating border cell clusters
In other contexts, such as in the eye and wing, Fz and Stbm are believed to
mediate intercellular communication via the formation of asymmetric protein
complexes at the adherens junctions, in which Fz in one cell is juxtaposed
with Stbm in the neighbouring cell
(Strutt, 2001;
Bastock et al., 2003). Because
the polar cells contact each other and the border cells via an adherens
junction-like region (Niewiadomska et al.,
1999), we studied whether Fz and Stbm localise to this region,
which would be consistent with the Fz/Stbm-dependent signalling that our
mosaic analysis revealed between these cells.
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We also observed Fz (but not Stbm) localised to the migratory edges of the
border cells, both prior to and during migration
(Fig. 5B,D). Fz localisation
has not previously been observed in migrating cells, but tagged forms of the
Xenopus Dsh homologue (a Fz-binding partner) are enriched at the
actin-rich bilateral tips of elongating cells undergoing convergent extension
(Kinoshita et al., 2003).
Using available reagents (Shimada et al.,
2001; Strutt et al.,
2006), we were unable to detect a specific distribution of
endogenous Dsh within migrating border cell clusters (data not shown).
Therefore, we investigated the distribution of a Dsh-GFP fusion protein, which
accurately reflects the junctional distribution of Dsh in the
Drosophila pupal wing (Axelrod,
2001). We found that this protein accumulated at high levels in a
punctate pattern in the cytoplasm of both polar follicle cells and border
cells (Fig. 5F,H). Although
there was evidence of enrichment in the junctional region of the clusters,
this was partly obscured by the high cytoplasmic levels. Similarly, we were
unable to determine whether Dsh-GFP was specifically localised to the
migratory edges of the border cells.
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DISCUSSION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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; De Calisto et al.,
2005; Heisenberg et al.,
2000; Jessen et al.,
2002; Montcouquiol et al.,
2003; Wallingford et al.,
2000; Phillips et al.,
2005; Weeraratna et al.,
2002). Many of these processes involve coordinated cell movement,
and yet this aspect of planar polarity pathway function is poorly
understood. Here, we use the Drosophila ovary to study the control of coordinated cell movements by the planar polarity pathway, taking advantage of its relative simplicity and the ability to precisely manipulate gene function in individual cell populations. Activity of the core polarity genes facilitates invasive migration of the border cell cluster through the nurse cells. Of particular interest is our observation that migration of the border cells is enhanced by planar polarity activity in the non-migratory epithelial polar follicle cells, suggesting a key role for interactions between migratory and non-migratory cell types.
In the Drosophila wing, the planar polarity pathway regionalises
cells via the formation of proximal and distal domains at the level of the
adherens junctions. The distal domain contains Fz
(Strutt, 2001), which acts via
the downstream factors Dsh (Axelrod,
2001) and RhoA (Strutt et al.,
1997) to ensure local production of a single actin-rich trichome,
while, in the proximal domain, Stbm
(Bastock et al., 2003) recruits
factors that locally inhibit trichome formation
(Adler et al., 2004)
(Fig. 6). During border cell
migration, the coordinated movement of the non-migratory polar follicle cells
and the migratory border cells is achieved in part by the border cells
retaining epithelial character in the region contacting the polar follicle
cells, but also having an actin-rich partly mesenchymal migratory region
(Niewiadomska et al., 1999).
Taking these observations together, we propose that, in border cells,
localised Fz in the migratory region and localised Stbm in the junctional
region might promote the production of actin-rich structures
(Fig. 6), which, in turn, would
increase the motility both of individual cells and the cluster as a whole.
Our mosaic analyses suggest a mechanism for how this localised Fz and Stbm activity is established within the border cells. Fz and Stbm mediate intercellular communication between the polar cells and the border cells via the production of junctional complexes. Because contact with an Fz-expressing polar cell enhances the migration of border cells, we surmise that Fz in each polar cell interacts with Stbm in the contacting border cell. Junctionally localised Stbm in the border cell can then act as a cue to indirectly promote actin-rich protrusion formation in the migratory region, at least in part via the localisation of Fz (Fig. 6).
Although the planar polarity pathway has been known for some years to
promote cell rearrangements during vertebrate gastrulation
(Wallingford et al., 2002),
surprisingly little is understood about its mechanisms of action in cell
movement and the particular roles of this pathway in cell-cell communication.
We have demonstrated that Fz/Stbm-mediated intercellular communication can
enhance the invasive migration of a group of cells. Migration of groups of
cells, sometimes including both motile and non-motile types, is important for
many processes in animal morphogenesis and in disease processes, such as
cancer metastasis (Friedl,
2004; Lecaudey and Gilmour,
2006). Our work provides evidence that planar polarity pathway
function could be generally important in coordinated cell migration, providing
a mechanism by which cells within a group can communicate and establish the
proper regional production of actin structures required for efficient
movement.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/134/17/3055/DC1
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ACKNOWLEDGMENTS |
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Footnotes |
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