Department of Genome Sciences, University of Washington, Box 357730, Seattle, WA 98195-7730, USA
* Author for correspondence (e-mail: berg{at}gs.washington.edu)
Accepted 10 September 2003
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SUMMARY |
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Key words: Oogenesis, Morphogenesis, bullwinkle, shark, Eggshell, Signaling
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Introduction |
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In Drosophila melanogaster, remodeling epithelia can interact with
an adjacent epithelium. Two well-studied examples include the migration of the
embryonic dorsal epithelium over the amnioserosa (reviewed by
Jacinto et al., 2002;
Knust, 1997
), and eversion of
leg and wing primordia relative to the peripodial tissue that bounds the
imaginal discs (reviewed by Fristrom,
1993
). These cell layers actively regulate the patterning and
movements of neighboring epithelia. Ablation of the peripodial membrane
results in growth and patterning defects in the eye and wing discs
(Gibson and Schubiger, 2000
).
In the embryo, the amnioserosa contributes signals
(Harden et al., 2002
;
Reed et al., 2001
;
Stronach and Perrimon, 2001
)
and mechanical force (Kiehart et al.,
2000
) to dorsal closure. During germband retraction, the
amnioserosa also signals to (Lamka and
Lipshitz, 1999
) and extends lamellipodia-like structures towards
(Schock and Perrimon, 2002
)
the retracting germband cells. We elaborate on a novel extracellular pathway
defined by bullwinkle (bwk)
(Rittenhouse and Berg, 1995
)
that is essential for proper tubulogenesis of the follicular epithelium during
synthesis of the dorsal appendages (DAs), specialized respiratory structures
of the eggshell. Additionally, we demonstrate that an adjacent squamous cell
layer acts as a substrate for the migrating epithelium and expresses factors
required for this morphogenetic process.
DA formation occurs within the context of the Drosophila egg
chamber, which consists of 650 somatically derived follicle cells
(Margolis and Spradling, 1995
)
surrounding a germline cyst composed of one oocyte and 15 nurse cells
(Spradling, 1993
). The germ
cells are interconnected via cytoplasmic bridges called ring canals, which
provide access for the transfer of nurse-cell material into the developing
oocyte. At stage 11, the nurse cells transport most of their cytoplasm into
the oocyte, and then undergo programmed cell-death
(Mahajan-Miklos and Cooley,
1994
). DA morphogenesis begins at stage 11, coincident with
nurse-cell apoptosis.
During DA formation, the somatic layer consists of two major populations
with distinctive morphologies, the stretch cells and columnar cells. At the
anterior, 50 squamous stretch cells cover the nurse cells. These cells
provide signals that pattern the anterior eggshell-forming cells and ensure
proper nurse-cell cytoplasmic dumping. The columnar cells overlie the oocyte
at the posterior and secrete the layers and specialized structures of the
eggshell (reviewed by Waring,
2000
). The anterior-most columnar cells (the centripetal cells)
migrate inwards, closing off the anterior end of the oocyte while synthesizing
the operculum and micropyle. In addition, two subpopulations of
65
dorsoanterior follicle cells form the two dorsal appendages through a complex
reshaping and reorganization of a flat epithelium into three-dimensional tubes
(Dorman et al., 2004
).
These DA-forming cells apically constrict and evert outwards, changing from a flat layer into tubular structures that extend anteriorly. Secretion of chorion proteins into the tube lumens creates the appendages (Fig. 1A). This process occurs during the final stages of oogenesis, downstream of the events that pattern the eggshell and embryonic axes.
|
The DA-forming cells require additional extracellular cues for normal
tubulogenesis. Mosaic analyses demonstrate that bwk is required in
the germline to regulate formation of the dorsal appendages
(Rittenhouse and Berg, 1995).
bwk encodes several SOX/TCF transcription factors with pleiotropic
functions (C.A.B., M. Terayama, D. H. Tran and K. Rittenhouse, unpublished),
regulating dorsal follicle-cell migration, anteroposterior (AP) patterning in
the embryo, and transport of nurse-cell cytoplasm into the oocyte. In
bwk mutants, the DA-forming cells not only fail to migrate
anteriorly, but instead extend much more laterally
(Dorman et al., 2004
), as
indicated by the wide DA paddle (Fig.
1B).
To elucidate the role of bwk in DA formation, we set out to
identify other components of this germline-to-soma signaling pathway. We
screened second-chromosome deficiencies for regions that genetically interact
with bwk. Tests of candidate mutations identified shark as a
strong Enhancer of bwk. shark encodes an SH2-ankyrin-repeat,
tyrosine-kinase protein (Ferrante et al.,
1995) that functions upstream of the JNK pathway during dorsal
closure of the embryo (Fernandez et al.,
2000
).
We show here that shark acts downstream of bwk in the squamous stretch cells and mediates the regulation of DA formation by bwk. Furthermore, detailed cellular analyses with stretch-cell markers show that the stretch cells provide a substrate for the DA-forming cells and appear morphogenetically active.
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Materials and methods |
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The Bloomington stock center provided the second-chromosome deficiency kit,
bsk1 and bskJ27, UAS-Src42.CA
(Tateno et al., 2000), and
FRT 42B tubP-GAL80 (Lee et al.,
2000
).
Deficiency screen
Second-chromosome deficiency stocks were crossed individually to
bwk strains in an F2 screen for dominant modifiers of the bwk DA
phenotype. Ten deficiency-bearing females were compared with ten siblings
lacking the deficiency in two bwk transheterozygous backgrounds,
bwk151/bwk8482 and
bwk151/bwkCT. Eggshell phenotypes were
counted daily for 3 days, without knowing the genotype until the end of the
counts.
We developed a numerical scoring system to facilitate identification of
dominant modifiers. The bwk mutants used in the screen produced a
range of phenotypes, which we sorted into four categories: wild type, short
thin, short broad and very short broad. Using a weighted average in which wild
type=4, short thin=3, short broad=2 and very short broad=1, we derived a score
from 4 to 1 as a composite of the phenotypic classes. Eggs from
bwk151/8482 females averaged a score of 1.43, while eggs
from bwk151/CT females averaged 2.96. The standard
deviation for both allelic combinations was 0.3. We scored eggs produced
by Df/+; bwk/bwk females and compared these values
to bwk/bwk siblings without the Df. Scores that
differed by more than one standard deviation (0.3) were considered evidence of
a significant interaction, while differences greater than 0.6 suggested strong
interactions.
In situ hybridization
We subcloned the BglII insert from a pCaSpeR-hs-shark
plasmid (Fernandez et al.,
2000) into pBluescript-SK and made digoxigenin-labeled
RNA probes using the Roche DIG-labeling kit. We followed a modified in situ
protocol (Tautz and Pfeifle,
1989
; Wasserman and Freeman,
1998
).
Immunofluorescence
We used the following primary antibodies: polyclonal rabbit anti-GFP
(Clonetech) and monoclonal mouse anti-GFP (Molecular Probes) both at 1/100;
rat anti-Fos (Riese et al.,
1997) and rabbit anti-c-Jun
(Chen et al., 2002
) both at
1/100; mouse monoclonal anti-ß-gal (Sigma) at 1/500. To detect the
primary antibodies we employed secondary antibodies conjugated to
Alexafluor488 and Alexafluor568 at 1/500 (Molecular Probes). We followed a
modified immunocytochemistry protocol
(French et al., 2003
).
Mosaic analyses
Clones were induced using the FLP/FRT method
(Chou and Perrimon, 1992;
Xu and Rubin, 1993
).
Heat-shock-driven FLP produced both germline and follicle-cell clones
(Golic and Lindquist, 1989
).
GAL4GR1 (a gift from Trudi Schüpbach), expressed in
follicle-cell stem cells and later-stage egg chambers, was used to induce
follicle-cell clones. Ubiquitin-GFP was used to mark the clones
(Davis et al., 1995
).
Positively marked clones were made with a modification of the MARCM method
(Lee et al., 2000). Females of
genotype hsFLP/+; FRT shark1/FRT
tubP-GAL80; UAS-GFPS65T/GAL4T155
were heat-shocked for 2 hours, dissected 3-4 days post-heat-shock, and stained
with anti-GFP.
Transgenic expression in bwk
UAS-shark+, UAS-bsk+ and
UAS-Src42A.CA+ were expressed using
GAL4c415, GAL455B or
GAL4CY2 in a bwk151/8482 background.
Eggs laid by 10 females per genotype were examined over 3 days on egg plates.
Control sibling flies lacking the GAL4 or UAS elements were also tested.
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Results |
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We employed two allelic combinations to facilitate isolation of both enhancers and suppressors: bwk151/8482, a strong loss-of-function combination (Fig. 1B), and bwk151/CT, a moderate loss-of-function combination. Both combinations produced a range of phenotypes. bwk151/8482 eggs have mainly short, broad dorsal appendages, facilitating the identification of suppressing mutations. bwk151/CT eggs manifest an array of DA structures from short, broad to long, tubular appendages. As bwk151/CT phenotypic profile exhibited a bias towards wild-type length DAs, this combination facilitated the isolation of enhancing interactions.
The Bloomington Stock Center maintains a large collection of deletions that
uncover 60-70% of the Drosophila genome. We screened 39 deficiencies
that uncover 78% of the second chromosome, as determined by
polytene-segment coverage (Table
1). We scored F2 progeny to examine the effect of these
deletions on the DA phenotypes of the two bwk-allele combinations.
Using a stringent scoring method (see Materials and methods), we identified
four deletions that exhibited a strong interaction, two enhancers and two
suppressors. Nine deletions exhibited a moderate interaction and seven
interacted weakly. We focused our initial efforts on the four strong
modifiers.
|
shark is a strong Enhancer of bwk
A mutation resulting in a premature stop codon in the shark gene
(Ferrante et al., 1995) showed
strong enhancement of the bwk phenotype, similar to the original deficiency
(data not shown). Germline clones of shark1, however,
failed to produce a detectable phenotype in oogenesis
(Fernandez et al., 2000
),
leading us to investigate a possible somatic function.
First, we examined expression of shark in oogenesis and noticed an unusual pattern (Fig. 2). shark transcript was present in the germline and somatic cells beginning in region 2 of the germarium (Fig. 2A). At the time of dorsal-appendage formation, egg chambers showed a pronounced pattern of discrete spots and tracks near the periphery of the nurse cells (Fig. 2C). These foci were often associated with stretch-cell nuclei (arrowheads, Fig. 2C'), suggesting that shark expression occurs in the thin (<1 µm) stretch-cell layer overlying the nurse cells. After stage 10, during rapid nurse-cell cytoplasmic transport, shark RNA levels increased dramatically in the nurse cells and the unusual foci were no longer readily visible (data not shown).
|
Stretch cells act as a substrate for DA formation
We examined egg chambers that expressed both stretch-cell-specific and
columnar-cell-specific markers. To label stretch cells, we employed the
GAL4/UAS system (Brand and Perrimon,
1993), driving UAS-GFPS65T with
GAL4c415 or GAL4A90
(Gustafson and Boulianne,
1996
; Manseau et al.,
1997
). c415 drives reporter expression in the stretch
cells while A90 labels both the stretch cells and the border cells.
To mark the DA-forming cells, we used the P[lacZ; ry+]
enhancer trap line PZ05650, which expresses highly in the
centripetally migrating columnar cells and in the two populations of
dorsoanterior follicle cells that synthesize the dorsal appendages
(Rittenhouse and Berg,
1995
).
At stage 10, the stretch cells covered the exterior of the nurse cells (Fig. 3A,B). The thinness of the layer meant that the cells were most visible at the junctions of nurse cells (Fig. 3A', blue arrowhead) and in regions surrounding the nuclei of the stretch cells (Fig. 3A', blue triangle). This morphology of the stretch cells, a significant thickening of the layer at discrete locations, could explain the shark RNA foci: localized cell thickening could cause ubiquitously expressed RNA to appear localized. Alternatively, the shark foci could represent actual localization of RNA within the stretch cells.
|
At stage 12, the nurse cells were much smaller due to transport of their cytoplasm into the oocyte (compare the nurse cells, labeled NC, in Fig. 3C with those in 3A), while the stretch cell layer had thickened. At this time, the stretch cells exhibited three interesting behaviors. First, in contrast to stage 10, the stretch cells enveloped all nurse cells (Fig. 3C). This envelopment could be due to an active movement or a byproduct of the nurse-cell shrinkage. Second, the migrating DA-forming cells moved over the stretch cells (green arrowhead, Fig. 3C). Finally, the stretch cells occasionally extended small cellular projections towards the DA-forming cells (arrow, Fig. 3E,F). By stage 13, the stretch cells resided between and underneath the two DA cell populations, which have reached the anterior end of the egg (data not shown).
These studies revealed that the stretch cells are a substrate for the
migrating DA-forming cells. This result contradicts a previous hypothesis
(King and Koch, 1963), who
proposed that the DA-forming cells migrated between the stretch and nurse
cells in an invasive manner. Thus, the stretch cells form an intervening layer
between the germ cells and the migrating DA-forming cells. The stretch cells
could express factors that mediate the movement of the DA cells across this
layer; shark may be such a factor, as suggested by the genetic
interaction and expression data. Because the known shark alleles are
lethal, we used mosaic analyses to examine the function of shark in
oogenesis.
shark clones exhibited DA defects in oogenesis
We induced clones with the shark1
(Fernandez et al., 2000) and
shark2 (R. Warrior, unpublished) alleles using the FLP/FRT
system (Xu and Rubin, 1993
).
We expressed FLP using either a heat-shock promoter-FLPase transgene
or a follicle-cell-specific GAL4 transgene, GR1, driving UAS-FLP.
GAL4GR1 is expressed in the follicle cells continuously from
the time of stem-cell division to stage 14 (T. Schüpbach, personal
communication). We marked the clonal cells in two fashions: negatively, such
that loss of Ubiquitin-GFP (Davis
et al., 1995
) defined homozygous shark cells, or
positively, with a modification of the MARCM/GAL80 method
(Lee et al., 2000
). In
positively marked clones, only homozygous shark cells expressed
UAS-GFPS65T (Amrein and
Axel, 1997
).
shark clones affected the morphology of the dorsal appendages and
the structure of the DA chorion (Fig.
4). In some eggs (Fig.
4A,E), the DA material appeared vacuolated, with gaps interposed
with a skeletal network. This phenotype resembled defects seen in mutants
affecting eggshell structure (reviewed by
Waring, 2000). In contrast to
chorion mutants, however, shark mosaic eggs with clones in the main
body had no obvious structural defect (data not shown).
|
The chorion and short-DA defects were not mutually exclusive; in fact, most chorion-defective appendages were also shortened. These defects were associated with clones in the anterior of the egg; when the entire anterior was clonal, both DAs were short and vacuolated (data not shown).
To establish the precise relationship between clone position and DA defect, we examined small clones and their effect on DA morphology. Scoring small clones by the absence of GFP proved difficult; however, once the DA cells had migrated onto the stretch cells. We used positively marked clones for clarity. In one representative clone, most GFP-positive clonal cells lay between the two DAs (Fig. 4C-G). By position, many of these marked cells should be stretch cells. Several of the GFP-positive cells were also closely associated with the chorion-defective DA, and likely label the DA-forming cells responsible for secreting the appendage chorion in E.
The frequency of these defects was low (Fig. 4H). Clone frequency, as measured by the number of egg chambers with at least one clone, for post-mitotic stages varied from 14.2 to 17.4%. No defects were seen with a wild-type FRT chromosome, while an FRT shark2 chromosome recapitulated the shark1 results. Most clones were made with the shark1 allele, where 7.5% of all stage-14 egg chambers showed a DA chorion defect and 1.9% had short DAs with normal DA chorion. We attribute this low frequency to several factors: regional specificity within the egg chamber, large clone-size requirement and incomplete penetrance for the short DA defect.
These studies showed that when a significant fraction of DA-cells was clonal, a chorion defect was seen. The large-clone-size requirement implied that neighboring shark+ cells could provide cell non-autonomous function for the homozygous shark cells. This effect was limited to the appendage associated with the clone; one DA could be affected while the other was normal.
The short-DA defects were, in turn, associated with large clones encompassing the stretch cells. These short-DA defects exhibited a variety of morphologies, from short and thin to short and broad like bwk mutant DAs. Furthermore, the short-DA defect was not fully penetrant; large clones in the stretch cells could result in mild defects.
To determine the relative contributions of these shark functions
in regards to bwk, we asked whether tissue-specific expression of a
wild-type shark+ transgene could ameliorate the DA defects
of a bwk mutant. As the stretch cells do not express or secrete
chorion (Margaritis et al.,
1980), we could distinguish between the role of shark in
chorion production versus DA migration.
Expression of UAS-shark+ suppresses
bwk
We postulated that bwk functioned to regulate shark
expression and/or activity in the stretch cells. Restoration of shark
expression in the stretch cells could compensate for loss of bwk, if
shark expression in these cells was a key downstream factor. To test
this hypothesis, we expressed UAS-shark+
(Fernandez et al., 2000) in a
bwk background using GAL4c415, which expresses
specifically in the stretch cells (Manseau
et al., 1997
), GAL455B, which expresses in
both the stretch cells and DA cells (Brand
and Perrimon, 1994
), and GAL4CY2, which
expresses in all follicle cells (Queenan
et al., 1997
).
Expression of a wild-type UAS-shark+ with the c415 and 55B drivers suppressed the bwk-mutant DA phenotype substantially (Fig. 5B; Table 2A), while CY2-driven expression had little effect (Table 2A). With stretch-cell-specific expression of UAS-shark, we generated a significant shift towards longer and more tubular DAs, a more wild-type-like phenotype. We quantified the suppression using a weighted average of four classes of DA phenotypes, where a difference of greater than or equal to 0.3 between the experimental and control scores indicated a significant interaction (see Materials and methods). The c415-driven suppression was equivalent to the strongest suppression observed in the deficiency-interaction screen. This result indicated that shark expression in the stretch cells is a key factor downstream of bwk. Additionally, the chorion function of shark was not crucial to the bwk DA phenotype. To explore shark function in the stretch cells, we assayed candidate factors that might act with shark in this tissue.
|
|
Expression of UAS-bsk+ led to a reduction in the number of eggs laid by bwk mothers but the morphology of the bwk DAs was not modified. Heterozygosity for two strong loss-of-function alleles (basket1 and basketJ27) also failed to interact with bwk (Table 2B). Additionally, expression and localization of both Jun and Fos were normal in bwk mutants or shark clones (Jun, Fig. 5C,D; Fos, J. Dorman and C.A.B., unpublished).
Another likely candidate gene expressed in the stretch cells is
dpp, partial overexpression of which can result in shortened and
fringed DAs (Twombly et al.,
1996). Expression of both dpp RNA and a dpp-lacZ
enhancer trap were normal in bwk mutants (data not shown).
Heterozygosity of dpp and/or its receptor failed to modify the strong
bwk151/8482 combination
(Table 2C), although modest
interactions occurred with the moderate bwk151/CT
combination (data not shown).
In mammalian cells, proteins related to Shark act alongside Src kinases in
mediating immunoreceptor signaling (Latour
and Veillette, 2001). We tested the Drosophila Src42A
gene for interaction with bwk. Src42A, like shark, functions
upstream of the JNK pathway in dorsal closure
(Tateno et al., 2000
).
Interestingly, Src42A mutations enhanced the moderate
bwk151/CT DA phenotype (Table
2D). Expression of transgenic UAS-Src42A.CA, an activated
form (Tateno et al., 2000
),
with the stretch-cell-specific GAL4c415 suppressed the
strong bwk DA phenotype (Table
2D). Compared with the UAS-shark suppression, the
UAS-Src42A.CA suppression was weaker but still produced a significant
shift towards longer DAs.
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Discussion |
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shark functions downstream of bwk
shark encodes a distinctive multidomain protein that regulates the
movements of epithelial cells in the dorsal embryonic epidermis
(Fernandez et al., 2000). This
non-receptor kinase is conserved, with homologs in Hydra
(Chan et al., 1994
) and sponge
(Suga et al., 1999
). The
mammalian counterparts contain homologous SH2 and tyrosine-kinase domains but
lack the ankyrin repeats (Chan et al.,
1991
; Taniguchi et al.,
1991
). These mammalian proteins, Zap70 and Syk, are recruited to
immunoreceptor complexes upon ligand binding and regulate immune-cell
activation and differentiation, functioning alongside Src kinases (reviewed by
Chu et al., 1998
). In T-cells,
Zap70 also mediates signaling downstream of integrin-receptor complexes that
feature in T-cell motility (Bearz et al.,
1999
; Soede et al.,
1998
).
We show that shark has two functions in oogenesis and that a bwk/shark pathway could involve the Shark and Src42A kinases in an evolutionarily conserved version of the mammalian signaling pathway.
shark function is required for DA structure and DA-cell
movement
Mosaic analyses with loss-of-function shark alleles established
two somatic functions in DA formation (Fig.
6). First, shark is required in the DA cells for proper
DA-chorion deposition, a complex process regulated at many levels (reviewed by
Waring, 2000). Mutations that
disrupt chorion-gene amplification or chorion-protein synthesis result in
thin, collapsed DAs and main-body eggshell
(Bauer and Waring, 1987
;
Landis et al., 1997
;
Mohler and Carroll, 1984
;
Nilson and Schüpbach,
1998
).
|
The second function of shark lies in the stretch cells and affects
the migration of the DA cells. Large stretch-cell clones resulted in shortened
DAs that varied in their morphology and penetrance. This variability could
result from residual activity of these mutant alleles (see Materials and
methods), non-cell autonomy, or functional redundancy. Although no Shark
paralogs are encoded in the genome (Adams
et al., 2000), several non-receptor tyrosine kinases share
homology in the SH2 and kinase domains, including Src42A.
In addition, stretch-cell expression of shark strongly suppressed the bwk-mutant DA phenotype, in concurrence with a direct role for bwk in regulating shark expression in this tissue. These results indicate that shark is key in regulating DA migration downstream of bwk. Full rescue was not likely achieved because of insufficient expression levels, the need to localize shark RNA, or the existence of shark-independent branches downstream of bwk.
These data suggest a model in which BWK regulates factors in the germline that are required for proper shark expression in the stretch cells. Shark then regulates the activity of targets required for DA-cell movement across the stretch-cell layer (Fig. 6A). Another factor that could be regulated by bwk is the Src42A kinase, which behaves similarly to shark (Fig. 6B). Loss of Src42A enhances bwk mutants, while stretch-cell expression of activated Src42A suppresses. Mammalian homologs of Shark function together with Src kinases, suggesting a conserved signaling cascade.
Stretch-cell signaling
Two other stretch-cell signaling pathways, JNK and DPP, regulate DA
morphogenesis. Tests with bwk and shark, however, failed to
reveal strong or definitive interactions. Loss of JNK activity in oogenesis
results in shortened and paddleless DAs, yet expression of
UAS-basket+ and reduction of bsk dose did not
alter the morphology of bwk eggshells. Furthermore, expression of the
AP-1 components was unaffected in bwk mutants and shark
clones. These data support the hypothesis that the bwk/shark
pathway does not primarily act through JNK signaling.
Moderate overexpression of dpp and loss of the type I receptors,
tkv and sax, can lead to shortened and somewhat broadened
DAs, resembling bwk mutants
(Twombly et al., 1996). The
expression of dpp RNA and a dpp enhancer trap, however, were
unaffected in bwk mutants. Both hypomorphic dpp alleles and
loss of type I receptors failed to interact with a strong bwk mutant.
Our data suggest that bwk does not directly regulate dpp
expression or activity but rather may modulate downstream targets.
Stretch-cell function
DA-cell movement over the stretch cells may require expression of
stretch-cell factors that guide or facilitate migration. As noted above,
mammalian proteins that share homology with Shark can bind to and regulate
integrin complexes. Shark may bind these and/or other adhesion receptors to
regulate cell migration either through signaling cues or by modulating the
extracellular matrix.
Shark could also regulate stretch cell behaviors, controlling the small
cellular projections that extend towards the DA cells during their anterior
movement. These extensions may guide or signal the DA-forming cells, as occurs
in imaginal discs (Cho et al.,
2000; Gibson and Schubiger,
2000
; Ramirez-Weber and
Kornberg, 1999
).
Extracellular signals and interactions are key components of morphogenetic processes. We have identified two downstream components of the bwk pathway that act in the stretch-cell layer to relay a novel germline signal required for the movement of a third tissue, the remodeling epithelium of the dorsal appendage cells.
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ACKNOWLEDGMENTS |
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