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First published online 21 January 2004
doi: 10.1242/dev.00989
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Howard Hughes Medical Institute, Molecular Biology Department, Washington Road, Princeton University, Princeton, NJ 08544, USA
* Author for correspondence (e-mail: ewieschaus{at}princeton.edu)
Accepted 17 November 2003
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SUMMARY |
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TOP
SUMMARY
Introduction
Materials and methods
Results
Discussion
REFERENCES |
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Key words: Drosophila, Cellularization, Blastoderm formation, Src64, Tec29, Scraps, Anillin, Bottleneck, Microfilament, Contractile
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Introduction |
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TOP
SUMMARY
Introduction
Materials and methods
Results
Discussion
REFERENCES |
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; Schejter and Wieschaus,
1993a). At the leading edge of membrane invagination, known as the
cellularization front, are stable infoldings of plasma membrane known as
furrow canals (Lecuit and Wieschaus,
2000; Fullilove and Jacobson,
1971). The base of each furrow canal is rich in the cytoskeletal
proteins F-actin and myosin II, and may provide a contractile force that helps
pull membrane inward (Schejter and
Wieschaus, 1993a; Young et
al., 1991; Warn and
Robert-Nicoud, 1990). To identify additional cytoskeleton
components involved in early embryogenesis, we used deficiencies to screen
part of the third chromosome (J.H.T. and E.W., unpublished). Analysis of the
genes that mapped to a region identified in this screen revealed a
cellularization phenotype associated with deletions in a Drosophila
src homolog, src64 (Src64B - FlyBase).
Src proteins have been shown to be involved in the regulation of the
cytoskeleton and its components during the reorganization of microfilaments in
both lamellipodia and filopodia in fibroblasts
(Frame et al., 2002;
Thomas and Brugge, 1997;
Thomas et al., 1995). The
structure of members of the Src family of consists of an N-terminal
myristoylation site, an SH3 domain, an SH2 domain, a tyrosine kinase domain
and a C-terminal regulatory domain. The myristoylation of Src protein allows
it to be tethered to the plasma membrane, whereas the SH3 and SH2 domains
serve to bind proline-rich recognition sequences and phosphotyrosine residues,
respectively (Harrison, 2003;
Frame, 2002;
Thomas and Brugge, 1997). In
vertebrates, Src has been shown to activate Tec family non-receptor tyrosine
kinases, which are similar to Src in that they have an SH3, an SH2 and a
kinase domain, and are also thought to interact with gene products associated
with the cytoskeleton (Smith et al.,
2001; Thomas and Brugge,
1997).
In Drosophila, there are two src homologs, src42
(Src42A - FlyBase) and src64, and one Tec family kinase
encoded by tec29 (Btk29A - FlyBase)
(Takahashi et al., 1996;
Katzen et al., 1990;
Vincent et al., 1989;
Gregory et al., 1987;
Wadsworth et al., 1985;
Simon et al., 1985;
Simon et al., 1983). There is
evidence that these genes play a role in cytoskeletal regulation. During
embryogenesis, for example, tec29 src42 double mutants and src42;
src64 double mutants have dorsal closure defects associated with reduced
quantities of phosphotyrosine and filamentous actin
(Tateno et al., 2000).
However, the best-studied example of src64 and tec29
involvement in cytoskeletal regulation is found in the formation and growth of
the ring canals during oogenesis. The ring canals are formed by the sequential
addition of several different proteins, including Src64 and Tec29, to an
actin- and anillin-rich arrested cleavage furrow left from the incomplete
divisions of the female germ cells (Sokol
and Cooley, 1999; Dodson et
al., 1998; Guarnieri et al.,
1998; Roulier et al.,
1998; Robinson and Cooley,
1996; Majajan-Miklos and Cooley, 1994;
Robinson et al., 1994). After
assembly and the loss of anillin localization, the ring canal enters a growth
phase (Robinson and Cooley,
1996). In src64 and tec29 mutants, ring canal
growth is stunted so that fully grown ring canals are never formed
(Dodson et al., 1998;
Guarnieri et al., 1998;
Roulier et al., 1998). The
ultimate consequence of Src activity may be the phosphorylation of Kelch, an
actin bundling protein that regulates actin polymerization by reversible
cross-linking (Kelso et al.,
2002; Tilney et al.,
1996).
Here we report that src64 and tec29 play a role in the cytoskeletal dynamics that occur during cellularization of the Drosophila embryo. src64 and tec29 are essential for the contraction of the microfilament rings that are present in the cellularization front, and appear to play a role in membrane invagination and in subsequent basal closure. This role is distinct from that of scraps (anillin), which is required for the formation of these rings but is not directly required for their contraction. Using double-mutant analysis, we show that a previously identified regulator of cellularization, bottleneck (bnk), acts by countering the src64-dependent contraction of the microfilament rings, but shows only an additive effect in combination with scraps. Finally, we propose a mechanical model for cellularization, taking into account the similar and different roles played by microfilament contraction and src64-independent forces.
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Materials and methods |
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TOP
SUMMARY
Introduction
Materials and methods
Results
Discussion
REFERENCES |
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) or
The Flybase Consortium (The Flybase
Consortium, 2003). src64
17 was
used as the src64 mutation in these experiments; it is a strong
reduction-of-function allele that eliminates most of the Src64 protein
(Dodson et al., 1998).
Df(3L)10H and Df(3L)Flex14
(Nose et al., 1994) were used
as the deficiencies for src64. tec29k00206 was
used as the tec29 allele as it eliminates the tec29
transcript, as assayed by in situ hybridization
(Roulier et al., 1998). Baba
et al. (Baba et al., 1999) and
Sinka et al. (Sinka et al.,
2002) report some tec29 activity in this mutant
suggesting that it is a strong reduction-of-function allele. Other alleles
used include scrapsRS and
scrapsPQ
(Schüpbach and Wieschaus,
1989), and Df(3R)tll-e to delete bnk
(Schejter and Wieschaus,
1993b).
tec29 germline clones were constructed essentially as previously
described (Roulier et al.,
1998; Guarnieri et al.,
1998). OreR males were crossed into tec29 germline clone
females to generate embryos.
Histology and image analysis
To visualize myosin, Even-skipped, Armadillo, Anillin and Bottleneck
proteins, embryos were methanol heat-fixed
(Wieschaus and Nusslein-Volhard,
1998) and stained with rabbit anti-myosin (a gift from C. Field,
Harvard Medical School, Boston, MA), guinea pig anti-Eve, mouse anti-Arm
(N27A1), rabbit anti-anillin (a gift from C. Field, Harvard Medical School,
Boston, MA) or rat anti-Bottleneck (5)
(Schejter and Wieschaus,
1993b) antibody, respectively. To visualize Tec29 protein and
phosphotyrosine-containing proteins, embryos were fixed in a
formaldehyde/phosphate buffer in the presence of heptane
(Oda et al., 1994) and stained
with either mouse anti-Tec29 (I19) antibody
(Roulier et al., 1998;
Vincent et al., 1989) or mouse
anti-phosphotyrosine (PY20) antibody (Transduction Laboratories, BD
Biosciences). Src64 protein was visualized by fixing embryos as described for
Tec29 protein, or by using 4% paraformaldehyde in lieu of formaldehyde and
staining with rabbit anti-Src64 antibody (a gift from T. Xu, Yale University,
New Haven, CT). Primary antibodies were detected with Alexa 488- and Alexa
546-conjugated goat antisera (Molecular Probes). Nuclei were visualized by
staining with Hoechst dye. Sagittal sections were obtained optically.
Cross-sections were made by using a 26-gauge hypodermic needle to manually cut
fixed and stained embryos. Embryos were mounted in Aquapolymount
(Polysciences), and were observed using a Nikon E800 fluorescence microscope
and a Zeiss LSM-510 confocal microscope.
Image analyses were performed using ImageJ software for Macintosh (W.
Rasband, NIH;
http://rsb.info.nih.gov/ij/).
Circularity was calculated by Image J software as the normalized ratio of area
to perimeter (c=4
A/p2, where c=circularity, A=area and
p=perimeter) so that in a true circle this ratio is one. The mean circularity
is reported as the circularity index. Samples were analyzed by calculating the
circularities of approximately 25 contiguous basal openings of embryos of the
same age and the results were compared using a t-test assuming
unequal sample variances. Subsamples of 20 contiguous basal openings were also
compared using a Wilcoxon-Mann-Whitney test. Genotypes were considered
different only if both tests produced P values of less than
0.001.
To analyze cellularization dynamics, six wild-type and six src64 embryos were mounted on biofoil membrane (Kendro) in halocarbon oil 27 (Sigma), covered with a coverslip supported by another coverslip on either side of the embryo and examined under bright field illumination using a Nikon E800 microscope. Time-lapse images were collected every 60 seconds using a CoolSNAP cf camera (Photometrics) and IPLab 3.6.3 image processing software for Macintosh (Scanalytics). Cellularization front depth was measured using ImageJ software.
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Results |
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TOP
SUMMARY
Introduction
Materials and methods
Results
Discussion
REFERENCES |
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). In addition to the reduced egg production, reduced hatch
rate and increased incidence of short embryos observed by Dodson et al.
(Dodson et al., 1998), we
observed that syncytial blastoderm stage src64 embryos also display a
weak nuclear fallout phenotype, such that some nuclei have dropped out of the
periphery before cellularization. This phenotype is much weaker than that
found in mutants such as nuf, SCAR and Arpc1
(Rothwell et al., 1998;
Zallen et al., 2002). We
examined older embryos of src6417
homozygous females for the level of Src64 expression and its intracellular
localization during cellularization. In wild-type embryos, Src64 protein
localizes most intensely to the cellularization front at the beginning of
cycle 14, in a domain that roughly overlaps that of other cytoskeletal
proteins such as anillin and myosin. Embryos from
src6417 homozygous females stained for
Src64 protein show no specific staining of the cellularization front and
essentially lack all non-background staining
(Fig. 1A,B).
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). In cross-sections of early cellularization stage wild-type
embryos, each furrow canal has a rounded appearance and adjacent furrow canals
are at a similar depth, giving the cellularization front a uniform and taut
appearance around the circumference of the embryo
(Fig. 2A). In
src6417 mutant embryos, the furrow canals
are less rounded, and adjacent furrow canals extend to different depths in the
embryo, giving the cellularization front a wavy, slack appearance as if it
were no longer under tension (Fig.
2B). Viewed from the surface, the early cellularization front in
wild-type embryos appears as a network of tightly apposed, densely staining
myosin microfilament rings surrounding the nuclei
(Fig. 2C). In
src6417 embryos, the microfilament rings
are not rounded but instead are irregular in shape and sometimes sharply
angular (Fig. 2D). We have used
the ImageJ circularity assay to estimate the tension of the microfilament
ring, based on the assumption that rings under tension will more closely
resemble a circle and will therefore have a circularity index close to 1.0 (W.
Rasband, NIH; see Materials and methods). During early cellularization, the
microfilament rings of the wild-type embryo have a circularity of 0.93
(Table 1). At the same stage in
src6417 embryos, the microfilament rings
enclose roughly the same area as those of wild type, but have a longer
perimeter such that the circularity ratio is 0.80
(Table 1), a significant
deviation from that of wild type (P<0.001). The longer perimeter
is the result of the microfilament ring having a convoluted and meandering
shape, such that indentations occur in the rings. The deviation from
circularity suggests that the microfilament rings are not under tension and
are held together in a loose mesh.
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). This contraction causes the lumen of the furrow
canals in wild-type embryos to expand into a flask-like shape
(Fig. 2E). The microfilament
rings are round and constricted (Fig.
2G), and have a circularity of 0.94
(Table 1). In
src6417 embryos the furrow canals do not
expand (Fig. 2F). The
microfilament rings are large, less rounded and convoluted
(Fig. 2H), they enclose a
greater area than the wild type (P<0.001) and have a circularity
index of 0.81 (Table 1), a
significant deviation from wild type (P<0.001). Membrane insertion during cellularization still proceeds in src64 embryos. The depth of membrane invagination and the dynamics of cellularization front ingression is similar to that of wild-type embryos (Fig. 3). These data suggest that src64-mediated microfilament contraction does not play a significant role in cellularization front invagination.
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; Guarnieri et
al., 1998; Roulier et al.,
1998). Cellularizing embryos derived from
tec29k00206 germline clones have large and
non-rounded microfilament rings like those of src64 embryos
(Fig. 4). tec29
microfilament rings have a circularity index of 0.82
(Table 1), similar to that of
src64 but very different from that of wild-type microfilament rings
(P<0.001). Tec29 protein is expressed at the cellularization front
and more weakly along the lateral cellular membrane in both wild-type embryos
and src6417 embryos, suggesting that
src64 does not act to localize Tec29 protein during cellularization
(Fig. 1C,D). This is in
contrast to the situation in the ovary where Src64 protein acts to localize
Tec29 protein to the ring canal (Guarnieri
et al., 1998; Roulier et al.,
1998). Phosphotyrosine staining is observed at the cellularization
front in both wild-type and src64 mutant embryos
(Fig. 1E,F). This suggests that
Src64 is not the major source of phosphotyrosine during cellularization as it
is in the egg chamber (Dodson et al.,
1998; Roulier et al.,
1998). Thus both src64 and tec29 are required
for microfilament ring contraction during cellularization, but tec29
is localized to the cellularization front independently of src64
activity.
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; The Flybase
Consortium, 2003) (Fig.
1E,F). During later development the anillin protein also localizes
to contractile rings during cytokinesis
(Field and Alberts, 1995).
Anillin is encoded by the gene scraps, which is defined by a maternal
effect lethal mutation (Schüpbach and
Wieschaus, 1989). We analyzed the phenotype of embryos from
mothers trans-heterozygous for two strong reduction-of-function mutations of
scraps (Schüpbach and
Wieschaus, 1989). The most informative phenotype of
scraps mutants is the absence of microfilament rings. This can be
readily seen by observing the density and continuity of myosin staining around
the basal openings in the cellularization front (compare
Fig. 5B with
Fig. 2C, and
Fig. 5D with
Fig. 2G). The furrow canals are
collapsed and lack the early bulb-like or the late flask-like morphology of
the wild type. Only some furrow canals show strong myosin staining
(Fig. 5A,C). Myosin is seen in
dense rod-like clumps lying between some of the basal cellular openings
(Fig. 5B,D). A similar
phenotype has been observed by C. Field (C. Field, personal communication).
This myosin distribution is similar to that of F-actin in the septin mutant
peanut during cellularization
(Adam et al., 2000), suggesting
that both anillin and certain septins play a role in the assembly or
maintenance of the microfilament rings.
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The premature contraction in bottleneck embryos does not require scraps (anillin)
We have used mutations in bottleneck (bnk) to define more
clearly the roles that src64 and scraps play in
cellularization. Bnk is a small, highly basic protein that regulates the
dynamic restructuring of the actin cytoskeleton so as to control the timing of
microfilament ring contraction during late cellularization. It is expressed
during early cellularization and its level drops precipitously during the
transition to the late phase (Schejter and
Wieschaus, 1993b). During early cellularization, Bnk co-localizes
with myosin, but extends further apically in the furrow canal
(Fig. 6).
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). The rings squeeze the nuclei into dumbbell shapes during
early cellularization, trapping and dragging some of them along with the
advancing cellularization front during late cellularization
(Fig. 7D) (Schejter and Wieschaus,
1993b). The microfilament rings of early cellularization and late
cellularization bnk embryos have circularity indices of 0.92 and 0.91
(Table 1), respectively, values
that do not differ from those of similarly staged wild-type embryos, even
though initially they enclose a much smaller area of open cytoplasm
(P<0.001).
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The hypercontraction caused by the absence of Bnk protein, coupled with the loss of structural integrity of the cellularization network caused by the absence of anillin and microfilament rings, leads to the apparent tearing of parts of the cellularization network. Several regions of the cytoskeleton are either stretched thin or broken, leaving large gaps in the cellularization front (Fig. 7C). This suggests that the loss of anillin and microfilament rings results in a fragile cytoskeletal structure that unravels in the absence of Bnk. These double-mutant results suggest that Bnk and anillin both play structural roles in the cellularization front, but that neither are necessary for microfilament contraction itself.
src64 is required for the premature contraction of bnk embryos
In restructuring the cytoskeleton during cellularization, Bnk controls the
timing of microfilament ring contraction so that basal closure does not occur
until after the cellularization front has passed the bases of the nuclei.
bnk mutants have a prematurely hyperconstricted ring phenotype
opposite to the non-constricted ring phenotype of src64 mutants.
src64 bnk double-mutant embryos look like src64 mutant
embryos. The src64 bnk embryos have the large, non-constricted
microfilament rings that appear to be under no tension
(Fig. 8). They have a
circularity index of 0.85 (Table
1), similar to that of src64 embryos but different from
that of bnk embryos (P<0.001). A few double-mutant
embryos showed some degree of microfilament ring contraction during late
cellularization; it is likely that these embryos are the result of some
residual activity of the reduction-of-function
src6417 allele. The analysis of src64
bnk double-mutant embryos demonstrates that the premature
hypercontraction of bnk requires src64 activity. The
interaction of bnk mutation with src64 and scraps
reveals the difference between the two genes: src64 is required for
microfilament contraction and scraps (anillin) is not. This suggests
that bnk regulates cytoskeletal contractility during cellularization
by counteracting the src64-mediated contraction of the microfilament
rings.
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Discussion |
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TOP
SUMMARY
Introduction
Materials and methods
Results
Discussion
REFERENCES |
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;
Tilney et al., 1996). It is
unlikely that myosin can play a role in this process as myosin-driven sliding
of actin filaments would lead to contraction rather than expansion
(Tilney et al., 1996).
Although myosin is localized to the ring canal, and null mutations in
regulatory myosin light chain cause defects in the ring canals, these defects
are not severe and do not prevent ring canal assembly or expansion
(Hudson and Cooley, 2002;
Jordan and Karess, 1997;
Edwards and Kiehart, 1996).
Thus, despite a similar involvement of src64 and tec29, it
is unlikely that microfilament ring constriction and ring canal expansion are
mechanistically similar.
scraps (anillin) is required for the formation of stable contractile microfilament rings
Anillin, which localizes to the cellularization front and shows higher
concentration in the contractile microfilament rings, is required for proper
cellularization. Anillin bundles actin filaments and may stabilize these
filaments during actin-myosin contraction
(Field and Alberts, 1995). On
the basis of these observations, we conclude that in the absence of anillin,
stable contractile microfilament rings do not form; instead the contractile
protein myosin is irregularly distributed in aggregates throughout the
cellularization front. Strikingly, loss of anillin in bnk embryos
does not suppress the severe early contraction defect seen in bnk
embryos. In the absence of the structure provided by these rings, the
contraction of the microfilaments is uneven, leading to increasing defects in
the shape of the basal openings as cellularization progresses. This suggests
that anillin is not required for the ability of the microfilaments of the
cellularization network to contract, only for their organization into stable
rings.
src64 and bnk oppose each other during early cellularization
The phenotypes presented in this paper support a model in which
src64 and bnk oppose each other to control contraction of
the early cellularization network. Double-mutant analysis reveals that
src64 is epistatic to bnk
(Fig. 9A). Bnk acts only to
restrain and partially redirect Src64-mediated ring constriction. The fact
that cellularization proceeds in src64 and tec29 mutants
suggests that a force other than microfilament ring contraction is sufficient
to drive cellularization front invagination. This force may be a result of the
insertion of membrane (Lecuit and
Wieschaus, 2000; Sisson et
al., 2000), or may be due to the action of plus-end directed
microtubular motors (Mazumdar and
Mazumdar, 2002; Foe et al.,
2000; Foe et al.,
1993), or some combination of both.
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As the cellularization front passes the bases of the nuclei and
cellularization shifts into its late phase of rapid progression
(Lecuit and Wieschaus, 2000),
Bnk expression is shut off and the protein is rapidly degraded and removed
from the cellularization network (Schejter
and Wieschaus, 1993b). In the absence of Bnk protein, there is no
force resisting microfilament ring contraction, so it no longer contributes to
driving cellularization front invagination. The src64-mediated force
is now directed along the radii of the rings, leading to their constriction.
This constriction pulls the membrane toward the center of the base of the
cell, expanding the furrow canals and leading to basal closure
(Fig. 9C). The
src64-independent force (membrane addition or microtubular motors)
may be the only force now driving the inward invagination of the
cellularization front.
In conclusion, our data define the differing roles that src64, tec29 and anillin play in the cytoskeletal dynamics of Drosophila cellularization, and reveal more precisely the role that the cytoskeleton plays in the formation of the cellular blastoderm. These data establish that microfilament ring organization and contraction are crucial to basal closure of the blastoderm cells during cellularization. However, these data also suggest that membrane invagination can proceed, though abnormally and less efficiently, in the absence of microfilament organization or contraction. It will be interesting to determine what the comparative roles and contributions of membrane insertion and microtubular motors are to the progression of the cellularization front.
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ACKNOWLEDGMENTS |
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REFERENCES |
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TOP
SUMMARY
Introduction
Materials and methods
Results
Discussion
REFERENCES |
|---|
Adam, J. C., Pringle, J. R. and Peifer, M.
(2000). Evidence for fundamental differentiation among
Drosophila septins in cytokinesis and cellularization.
Mol. Biol. Cell 11,3123
-3135.
Baba, K., Takeshita, A., Majima, K., Ueda, R., Kondo, S., Juni,
N. and Yamamoto, D. (1999). The Drosophila
Bruton's tyrosine kinase (Btk) homolog is required for adult survival and male
genital formation. Mol. Cell. Biol.
19,4405
-4413.
Dodson, G. S., Guarnieri, D. J. and Simon, M. A.
(1998). Src64 is required for ovarian ring canal
morphogenesis during Drosophila oogenesis.
Development 125,2883
-2892.[Abstract]
Edwards, K. A. and Kiehart, D. P. (1996).
Drosophila nonmuscle myosin II has multiple essential roles in
imaginal disc and egg chamber morphogenesis.
Development 122,1499
-1511.[Abstract]
Field, C. M. and Alberts, B. M. (1995).
Anillin, a contractile ring protein that cycles from the nucleus to the cell
cortex. J. Cell Biol.
131,165
-178.
The Flybase Consortium (2003). The flybase
database of the Drosophila genome projects and community literature.
Nucl. Acids Res. 31,172
-175.
Foe, V. E., Odell, G. M. and Edgar, B. A.
(1993). Mitosis and morphogenesis in the Drosophila
embryo: point and counterpoint. In The Development of
Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp.149
-300. Cold Spring Harbor, NY: Cold Spring Harbor
Laboratory Press.
Foe, V. E., Field, C. M. and Odell, G. M.
(2000). Microtubules and mitotic cycle phase modulate
spatiotemporal distributions of F-actin and myosin II in Drosophila
syncytial blastoderm embryos. Development
127,1767
-1787.[Abstract]
Frame, M. C. (2002). Src in cancer:
deregulation and consequences for cell behavior. Biochim. Biophys.
Acta 1602,114
-130.[Medline]
Frame, M. C., Fincham, V. J., Carragher, N. O. and Wyke, J.
A. (2002). v-src's hold over actin and cell
adhesion. Nat. Rev. Mol. Cell Biol.
3, 233-245.[CrossRef][Medline]
Fullilove, S. L. and Jacobson. A. G. (1971).
Nuclear elongation and cytokinesis in Drosophila montana.
Dev. Biol. 26,560
-570.[CrossRef][Medline]
Gregory, R. J., Kammermeyer, K. L., Vincent, W. S., III and
Wadsworth, S. G. (1987). Primary sequence and
developmental expression of a novel Drosophila melanogaster src gene.
Mol. Cell. Biol. 7,2119
-2127.
Guarnieri, D. J., Dodson, G. S. and Simon, M. A.
(1998). Src64 regulates the localization of a Tec-family
kinase required for Drosophila ring canal growth. Mol.
Cell 1,831
-840.[CrossRef][Medline]
Harrison, S. C. (2003). Variation on a Src-like
theme. Cell 112,727
-740.
Hudson, A. M. and Cooley, L. (2002).
Understanding the function of actin-binding proteins through genetic analysis
of Drosophila oogenesis. Annu. Rev. Genet.
36,455
-488.[CrossRef][Medline]
Jordan, P. and Karess, R. (1997). Myosin light
chain-activating phosphorylation sites are required for oogenesis in
Drosophila. J. Cell Biol.
139,1805
-1819.
Katzen, A. L., Kornberg, T. and Bishop, J. M.
(1990). Diverse expression of dsrc29A, a gene related to
src, during the life cycle of Drosophila melanogaster.
Development 110,1169
-1183.
Kelso, R. J., Hudson, A. M. and Cooley, L.
(2002). Drosophila Kelch regulates actin organization
via Src64-dependent tyrosine phosphorylation. J. Cell
Biol. 156,703
-713.
Lecuit, T. and Wieschaus, E. (2000). Polarized
insertion of new membrane from a cytoplasmic reservoir during cleavage of the
Drosophila embryo. J. Cell Biol.
150,849
-860.
Lindsley, D. L. and Zimm, G. A. (1992).The genome of Drosophila melanogaster
. San Diego:
Academic Press.
Mahajan-Miklos, S. and Cooley, L. (1994).
Intercellular cytoplasm transport during Drosophila oogenesis.
Dev. Biol. 165,336
-351.[CrossRef][Medline]
Mazumdar, A. and Mazumdar, M. (2002). How one
becomes many: blastoderm cellularization in Drosophila melanogaster.
BioEssays 24,1012
-1022.[CrossRef][Medline]
Nose, A., Takeichi, M. and Goodman, C. S.
(1994). Ectopic expression of Connectin reveals a repulsive
function during growth cone guidance and synapse formation.
Neuron 13,525
-539.[CrossRef][Medline]
Oda, H., Uemura, T., Harada, Y., Iwai, Y. and Takeichi, M.
(1994). A Drosophila homolog of cadherin associated with
armadillo and essential for embryonic cell-cell adhesion. Dev.
Biol. 165,716
-726.[CrossRef][Medline]
Robinson, D. N., Cant, K. and Cooley, L.
(1994). Morphogenesis of Drosophila ovarian ring canals.
Development 120,2015
-2025.[Abstract]
Robinson, D. N. and Cooley, L. (1996). Stable
intercellular bridges in development: the cytoskeleton lining the tunnel.
Trends Cell Biol. 6,474
-479.[CrossRef][Medline]
Rothwell, W. F., Fogarty, P., Field, C. M. and Sullivan, W.
(1998). Nuclear fallout, a Drosophila protein that
cycles from the cytoplasm to the centrosomes, regulates cortical microfilament
organization. Development
125,1295
-1303.[Abstract]
Roulier, E. M., Panzer, S. and Beckendorf, S. K.
(1998). The Tec29 tyrosine kinase is required during
Drosophila embryogenesis and interacts with Src64 in ring canal
development. Mol. Cell
1, 819-829.[CrossRef][Medline]
Schejter, E. D. and Wieschaus, E. (1993a).
Functional elements of the cytoskeleton in the early Drosophila
embryo. Annu. Rev. Cell Biol.
9, 67-99.[CrossRef][Medline]
Schejter, E. D. and Wieschaus, E. (1993b).
bottleneck acts as a regulator of the microfilament network governing
cellularization of the Drosophila embryo.
Cell 75,373
-385.[CrossRef][Medline]
Schüpbach, T. and Wieschaus, E. (1989).
Female sterile mutations on the second chromosome of Drosophila
melanogaster. I. Maternal effect mutations.
Genetics 121,101
-117.
Simon, M. A., Kornberg, T. and Bishop, J. M.
(1983). Three loci related to the src oncogene and
tyrosine-specific protein kinase activity in Drosophila.
Nature 302,837
-839.[CrossRef][Medline]
Simon, M. A., Drees, B., Kornberg, T. and Bishop, J. M.
(1985). The nucleotide sequence and the tissue-specific
expression of Drosophila c-src. Cell
42,831
-840.[CrossRef][Medline]
Sinka, R., Jankovics, F., Somogyi, K., Szlanka, T.,
Lukácsovich, T. and Erdélyi, M. (2002).
poirot, a new regulatory gene of Drosophila oskar acts at
the level of the short Oskar protein isoform.
Development 129,3469
-3478.
Sisson, J. C., Field, C., Ventura, R., Royou, A. and Sullivan,
W. (2000). Lava Lamp, a novel peripheral golgi protein, is
required for Drosophila melanogaster cellularization. J.
Cell Biol. 151,905
-917.
Smith, C. I. E., Islam, T. C., Mattsson, P. T., Mohamed, A. J.,
Nore, B. F. and Vihinen, M. (2001). The Tec family of
cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs
in other species. BioEssays
23,436
-446.[CrossRef][Medline]
Sokol, N. S. and Cooley, L. (1999).
Drosophila Filamin encoded by the cheerio locus is a
component of ovarian ring canal. Curr. Biol.
9,1221
-1230.[CrossRef][Medline]
Takahashi, F., Endo, S., Kojima, T. and Saigo, K.
(1996). Regulation of cell-cell contacts in developing
Drosophila eyes by Dsrc41, a new, close relative of
vertebrate c-src. Genes Dev.
10,1645
-1656.
Tateno, M., Nishida, Y. and Adachi-Yamada, T.
(2000). Regulation of JNK by Src during Drosophila
development. Science
287,324
-327.
Thomas, S. M., Soriano, P. and Imamoto, A.
(1995). Specific and redundant roles of Src and Fyn in organizing
the cytoskeleton. Nature
376,267
-271.[CrossRef][Medline]
Thomas, S. M. and Brugge, J. S. (1997).
Cellular functions regulated by Src family kinases. Annu. Rev. Cell
Dev. Biol. 13,513
-609.[CrossRef][Medline]
Tilney, L. G., Tilney, M. S. and Guild, G. M.
(1996). Formation of actin filament bundles in the ring canals of
developing Drosophila follicles. J. Cell
Biol. 133,61
-74.
Vincent, W. S., III, Gregory, R. J. and Wadsworth, S. C.
(1989). Embryonic expression of a Drosophila src gene:
alternate forms of the protein are expressed in segmented stripes and in the
nervous system. Genes Dev.
3, 334-347.
Wadsworth, S. C., Madhavan, K. and Bilodeau-Wentworth, D.
(1985). Maternal inheritance of transcripts from three
Drosophila src-related genes. Nucl. Acids
Res. 13,2153
-2170.
Warn, R. M. and Robert-Nicoud, M. (1990).
F-actin organization during the cellularization of the Drosophila
embryo as revealed with a confocal laser scanning microscope. J.
Cell Sci. 96,35
-42.
Wieschaus, E. and Nusslein-Volhard, C. (1998).
Looking at embryos. In Drosophila: A Practical
Approach, 2nd edn (ed. D. B. Roberts), pp.179
-214. Oxford: Oxford University Press.
Young, P. E., Pesacreta, T. C. and Kiehart, D. P.
(1991). Dynamic changes in the distribution of cytoplasmic myosin
during Drosophila embryogenesis. Development
111, 1-14.[Abstract]
Zallen, J. A., Cohen, Y., Hudson, A. M., Cooley, L., Wieshaus,
E. and Schejter, E. D. (2002). SCAR is a primary
regulator of Arp2/3-dependent morphological events in Drosophila.
J. Cell Biol. 156,689
-701.
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