Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370, USA
* Author for correspondence (e-mail: wumin{at}bio.fsu.edu)
Accepted 28 July 2005
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SUMMARY |
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Key words: cut, Endocycle, Cell cycle transition, Notch signaling, Drosophila melanogaster
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Introduction |
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The Notch pathway has a wide range of biological roles in
Drosophila development. Notably, it is implicated in a lateral
inhibition process during neurogenesis that restricts sensory-organ formation
and boundary formation in the wing imaginal disc
(Beatus and Lendahl, 1998;
Bray, 1998
). In oogenesis,
Notch signaling has been shown to be implicated in the specification of the
polar follicle cells and regulation of cell-cycle programs in the
follicle-cell epithelium (Althauser et al.,
2005
; Deng et al.,
2001
; Grammont and Irvine,
2001
; Lopez-Schier and St
Johnston, 2001
; Ruohola et
al., 1991
; Torres et al.,
2003
).
Drosophila oogenesis is a highly regulated developmental process
[for a review of oogenesis, see Spradling
(Spradling, 1993)]. During
oogenesis, the somatically derived follicle cells and the germline cells
communicate with each other; disruption of the development of one invariably
affects the other. This tightly regulated mutual differentiation process
serves as an excellent model for the study of cell-cell communication and
temporal and spatial control of cell differentiation
(Deng and Bownes, 1998
).
During oogenesis, the main-body follicle cells undergo three different modes
of cell cycle as they develop. From the germarium to stage 6, these cells
undergo an archetypal mitotic cycle that includes complete G1, S, G2 and M
phases (Fig. 1A), during which
the expression of mitotic markers, such as G2 cyclins, Cyclin A (CycA) and
Cyclin B (CycB), and phosphohistone 3 (PH3), oscillates
(Deng et al., 2001
;
Schaeffer et al., 2004
)
(Fig. 1B). Beginning at around
stage 7, main-body follicle cells undergo three rounds of the endocycle (also
called endoreplication or the endoreduplication cycle), which includes only
the G and S phases (Edgar and Orr-Weaver,
2001
; Lee and Orr-Weaver,
2003
) (Fig. 1A). As
a result, 16 copies of genomic DNA are present in each nucleus. The switch
from the mitotic cycle to the endocycle is marked by abrupt disappearance of
mitotic cyclins and PH3 (Bradbury,
1992
; Deng et al.,
2001
; Hendzel et al.,
1997
). Endocycle cells retain oscillating patterns of expression
of Cyclin E (CycE) and genomic 5-bromo-2-deoxyuridine (BrdU) incorporation
(Follette et al., 1998
).
Coupled with the switch from the mitotic cycle to the endocycle, follicle
cells show downregulation of immature-cell-fate markers such as Fasciclin III
(FasIII); this downregulation could serve as a marker for follicle-cell
differentiation (Lopez-Schier and St
Johnston, 2001
). At stage 10B, main-body follicle cells exit the
endocycle and undergo amplification of specific genomic regions (e.g. the
chorion gene region; this stage could therefore be referred to as the
chorion-gene amplification or amplification stage;
Fig. 1A)
(Calvi et al., 1998
;
Cayirlioglu et al., 2001
).
The switch from the mitotic cycle to the endocycle is induced by Notch
signaling (Deng et al., 2001;
Lopez-Schier and St Johnston,
2001
). At around stage 6 of oogenesis, Dl expression is elevated
in the germline cells, coincident with the transition from the mitotic cycle
to the endocycle and downregulation of FasIII. Indeed, removal of Dl
function in the germline cells or Notch function in the follicle
cells keeps follicle cells in the mitotic cycle during mid-oogenesis (stages 7
to 10A). In addition, the immature follicle-cell-fate marker, FasIII, remains
expressed at a high level in these cells. Notch-dependent cell-cycle
transition and cell differentiation require protein cleavage, as
-secretase components Presenilin (Psn) and Nicastrin are involved in
this process (Lopez-Schier and St
Johnston, 2001
; Lopez-Schier
and St Johnston, 2002
). In addition, the nuclear effector of Notch
signaling, Su(H), is needed for the switch
(Deng et al., 2001
;
Lopez-Schier and St Johnston,
2001
). Notch signaling negatively regulates String (Stg)/cdc25
phosphatase and G2 cyclins and positively regulates Fizzy-related/Hec1/Cdh1
(Fzr) (Deng et al., 2001
;
Schaeffer et al., 2004
;
Shcherbata et al., 2004
). Fzr,
also known as Retina aberrant in pattern, is a conserved WD domain protein.
Previous studies have shown that Fzr is required for degeneration of G2
cyclins in an anaphase promoting complex/cyclosome (APC/C) E3 ligase-dependent
manner. Loss of fzr function in Drosophila follicle cells
causes defects in the mitotic-to-endocycle transition and results in the
maintenance of CycA expression after stage 6 during oogenesis
(Schaeffer et al., 2004
).
Cut is a DNA binding protein that contains a unique homeodomain and three
Cut repeats (Nepveu, 2001).
Its expression and function have been characterized in several developmental
processes in Drosophila. In wing imaginal discs, it is induced by
Notch signaling at the dorsal-ventral (DV) border to maintain the DV boundary
(de Celis and Bray, 1997
;
de Celis et al., 1996
). During
neurogenesis, Cut is involved in sensory organ differentiation, a process for
which Notch function is also required
(Blochlinger et al., 1991
;
Brewster et al., 2001
). In
addition, Cut expression has been found in follicle cells. It is required for
egg-chamber encapsulation and coordination of the germline and follicle-cell
differentiation (Jackson and Blochlinger,
1997
). Cut homologues have been identified in vertebrates, e.g.
the CCAAT displacement protein (CDP)
(Nepveu, 2001
). Unlike its
Drosophila homologue, vertebrate Cut is known to be involved in
cell-cycle progression in some cell types
(Coqueret et al., 1998
). Here
we show that, in Drosophila follicle cells, Cut also regulates the
cell cycle, a function that may have been conserved during evolution.
Our data show that Cut expression is downregulated by the Notch pathway in follicle cells during mid-oogenesis and that the downregulation is necessary for proper entry of follicle cells into the endocycle and for their differentiation. In our experiments, loss of cut function resulted in premature entry into the endocycle and cell-autonomous differentiation. Cut promoted CycA expression by negatively regulating Fzr. Our results suggest that Cut functions as a linker between Notch and genes that are involved in cell-cycle progression and cell differentiation.
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Materials and methods |
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Generation of follicle cell and germline clones
Fly culture and crosses were performed according to standard procedures.
Mutant clones were generated by mitotic recombination with the FLP/FRT system
(Xu and Rubin, 1993) by either
X-chromosome or third-chromosome heat-shock-inducible flipase (hsFLP). After
heat shock, all flies were put in fresh food vials with wet yeast for 1-2 days
before dissection. Clones were marked with ubi-GFP or histone-GFP (hGFP)
(Maines et al., 2004
). To
obtain germline clones, we heat shocked flies as second- and third-instar
larvae for 2 hours at 37°C (Deng and
Ruohola-Baker, 2000
). For follicle cell clones, 1- to 5-day-old
flies were heat shocked as adults for 1 hour at 37°C and put into fresh
food vials. For generation of Cut mutant clones in early-stage egg chambers,
flies were dissected 1-2 days after heat shock. For generation of flip-out
Gal4 overexpression clones, adult flies were heat shocked for 45 minutes and
put into fresh food vials for 2-3 days before dissection.
Immunocytochemistry and BrdU labeling
Immunocytochemistry was carried out as described previously
(Deng et al., 2001). The
following antibodies were used: mouse anti-FasIII 1:15, mouse anti-CycB 1:5,
mouse anti-Cut 1:15, mouse anti-Eya 1:10 (Developmental Studies Hybridoma
Bank; DSHB), mouse anti-BrdU 1:50 (BD Bioscience), rabbit anti-ORC2 1:3000 (a
gift from S. P. Bell) (Royzman et al.,
1999
), rabbit anti-Bib 1:2000 (a gift from Y. Jan), rabbit
anti-PH3 1:200 (Upstate Biotechnology, NY, USA), rabbit anti-CycA 1:500 (a
gift from C. Lehner), rabbit anti-ß-galactosidase 1:5000 (Sigma), guinea
pig anti-CycE 1:500 (a gift from T. Orr-Weaver), Alexa Fluor 546 goat
anti-guinea pig, Alexa Fluor 546 or 633 goat anti-mouse (1:500), and Alexa
Fluor 488, 546 or 633 goat anti-rabbit (1:500) (Molecular Probes). Images were
acquired with a Zeiss LSM 510 confocal microscope and assembled in Adobe
Photoshop.
BrdU labeling was carried out as described by Calvi et al.
(Calvi et al., 1998), with the
following modifications. Dissected ovaries were incubated in 0.5 mg/ml BrdU
(Sigma) in Grace's medium (Mediatech-Cellgro, VA) for 1 hour at room
temperature, followed by fixation in EM-grade formaldehyde/buffer
B/dH2O (1:1:4) for 15 minutes. Ovaries were then washed twice (15
minutes each rinse) in PBS + 0.4% Triton X-100, twice (15 minutes each rinse)
in DNase I reaction buffer (66 mM Tris, pH 7.5, 5 mM MgCl2, 1 mM
fresh 2-mercaptoethanol), and incubated in 12 µl DNase I (25 mg/ml)/1 ml
DNase reaction buffer at 37°C for 45 minutes, washed three times (1 minute
each wash) then once more (15 minutes) in PBT, and blocked in PBT with 5%
normal goat serum overnight at 4°C. BrdU was detected with the mouse
anti-BrdU antibody described above.
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Results |
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Because downregulation of Cut expression in main-body follicle cells was
coupled with the switch from the mitotic cycle to the endocycle, a process
induced by Notch signaling, we hypothesized that the Notch pathway negatively
regulates Cut during the cell-cycle switch. To test this hypothesis, we first
generated Dl germline clones using the FLP/FRT-induced mitotic
recombination technique (Xu and Rubin,
1993). In follicle cells that surrounded the Dl germline
clone, Cut was continuously expressed after stage 6
(Fig. 2A,A'). Next, we
examined Cut expression in Notch follicle-cell clones, as Notch is
required cell-autonomously in follicle cells for the mitotic cycle/endocycle
switch (Deng et al., 2001
;
Lopez-Schier and St Johnston,
2001
). As expected, in egg chambers older than stage 6,
Notch mutant follicle cells upregulated Cut expression in a
cell-autonomous fashion, whereas their wild-type neighbors showed no Cut
expression (Fig. 2B,B').
In addition to Notch, psn and Su(H) clones resulted in
upregulated Cut expression in egg chambers beyond stage 6
(Fig. 2C,C',D,D'),
but Su(H) clones had a less severe effect in regulating Cut
expression. Cut expression was rarely detected in Su(H) clones in
stage 9 or 10A egg chambers, but its expression was very common in
Notch and psn clones (data not shown). Nonetheless, the
findings that Dl germline clones and Notch, psn and
Su(H) follicle-cell clones all induced Cut expression during
mid-oogenesis suggest that the canonical Notch pathway is required for
downregulation of Cut expression at the mitotic cycle/endocycle switch.
|
Next, we investigated whether ctdb7 mutant cells
undergo the endocycle after exiting the mitotic cycle. CycE expression and
BrdU incorporation oscillate in endocycle cells
(Edgar and Orr-Weaver, 2001).
In ctdb7 follicle-cell clones from stages 4-6, CycE
staining was detected in a sporadic pattern
(Fig. 3D,D'). In
addition, we observed BrdU incorporation in some of these mutant cells (data
not shown). Oscillation of CycE and BrdU incorporation and lack of CycA, CycB
and PH3 staining in cut clones suggest that the mutant cells
precociously entered the endocycle.
Next, we set out to determine whether the cut mutant cells switched from the endocycle to gene amplification correctly. These cells appeared to incorporate BrdU in a foci-like pattern similar to that of their wild-type neighbors (Fig. 3E,E'). This result suggests that the switch from the endocycle to amplification was not affected, which also indicates that late Cut expression, starting at stage 10B (Fig. 1B), in follicle cells is not essential for chorion gene amplification.
Prolonged Cut expression during mid-oogenesis causes defects in the mitotic cycle/endocycle switch
Because Cut was required for follicle-cell proliferation and its expression
was downregulated by Notch signaling upon entry into the endocycle, we set out
to determine whether extending Cut expression beyond stage 6 could maintain
the follicle cells in a mitotic cycle. Ectopic Cut expression in follicle
cells after stage 6 was achieved by means of the flip-out Gal4/UAS
technique. DAPI staining showed that Cut-misexpressing cells had slightly
smaller nuclei than their wild-type neighbors
(Fig. 4A,A'). These cells
also appeared to be more densely distributed, a phenotype resembling that of
the Notch clones (Deng et al.,
2001). To determine whether these cells exhibited features of a
mitotic cycle, we applied a series of cell-cycle markers to stain the mosaic
egg chambers. Interestingly, we found that 62% of egg chambers with
Cut-misexpressing follicle cells between stages 7 and 8 showed CycA expression
(Fig. 4B,B'; n=100; on average, 2% of cut-expressing cells showed CycA
expression), whereas wild-type follicle cells showed no CycA expression during
these stages. This result indicates that prolonged expression of Cut caused a
defect in the mitotic cycle/endocycle switch in follicle cells. The M-phase
marker PH3, however, was not apparent in any of the Cut-misexpressing clones
during stages 7-10 (data not shown), suggesting that these cells did not enter
M phase or complete a mitotic cycle although they maintained CycA
expression.
|
To induce the mitotic cycle/endocycle switch, Notch signaling not only
promotes M phase exit by upregulating Fzr, it also suppresses Stg, a CDC25
homolog required for G2/M progression
(Edgar et al., 1994;
Kumagai and Dunphy, 1991
).
Although misexpression of Cut downregulated Fzr, it did not seem to be able to
regulate stg expression. A stg-lacZ reporter gene showed no
change of expression in Cut-misexpressing cells
(Fig. 4D,D'), but
misexpression of both Stg and Cut in follicle cells at stages 7-8 could drive
an extra round of cell cycle, as shown by PH3 staining in some GFP-positive
cells (Fig. 4E,E'; 60% of
egg chambers counted had PH3-positive cells; n=70). In contrast,
misexpression of either Cut or Stg alone was not able to drive an extra round
of cell division (data not shown).
To determine whether cells with prolonged Cut expression would proceed to
gene amplification, we examined BrdU incorporation and ORC2 and CycE staining
in mosaic egg chambers. In wild-type cells, ORC2, a component of the origin
recognition complex, is colocalized at the BrdU incorporation foci in cells
undergoing chorion gene amplification (Fig.
4F,F',F'') (Royzman
et al., 1999). In these cells, CycE showed a uniform pattern at
about the same stage (Fig.
4G,G'). In Cut-misexpressing cells, the foci-like BrdU
incorporation and ORC2 staining pattern was not detected, and CycE expression
was also missing (Fig. 4F,G).
Taken together, these data indicate that Cut misexpression does not allow the
follicle cells to switch properly into the endocycle, and these cells are also
unable to undergo gene amplification.
|
Interestingly, persistent Cut misexpression/overexpression beyond stage 10 eventually led to a polar-cell fate. In a stage 12 egg chamber, Cut-positive cells no longer expressed Eya (Fig. 5F,F'); instead, the polar-cell fate marker A101 was expressed (Fig. 5G,G').
To determine whether Cut is required in main-body follicle cells to
maintain an undifferentiated fate, we examined the expression of FasIII and
Eya in transient ctdb7 clones at stages 4-6. In most
cases, FasIII expression was downregulated at the basal-lateral surface of the
follicle cells (Fig.
6A,A',B,B'), but at the apical-lateral region, FasIII
expression was still detected (Fig.
6B,B', arrowhead). To determine whether this type of FasIII
staining is normally present, we re-examined the expression pattern of FasIII
in wild-type follicle cells. Surprisingly, an apical-lateral staining of
FasIII was detected in wild-type follicle cells during stages 7-9
(Fig. 6C,C'), in contrast
to its location along the entire lateral membrane during earlier stages
(Fig. 6D,D'). We
therefore concluded that the restriction of FasIII to the apical-lateral
membrane reflected follicle-cell differentiation and that cut
mutation caused follicle cells to differentiate prematurely. This conclusion
was supported by staining for Eya in cut follicle-cell clones, which
showed cell-autonomous loss of Eya expression
(Fig. 6E,E',F,F').
Lack of Eya is shown in differentiated columnar cells and the polar cells
during oogenesis (Bai and Montell,
2002). A polar cell fate marker, PZ80, was not expressed
in the clone (Fig. 6F),
revealing that these cells did not take the polar-cell fate. Together, these
results suggest that cut mutant follicle cells show a differentiated
fate and that cut is required to maintain the follicle cells in an
immature stage in early oogenesis.
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Discussion |
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Interaction between the Notch pathway and Cut
Several roles for cut during Drosophila oogenesis have
been described (Jackson and Blochlinger,
1997). First, cut negatively interacts with
Notch for partitioning of individual germline cysts into egg
chambers. Second, cut defines a signaling pathway from the follicle
cells to the oocyte to maintain the germline integrity. In addition, the
rarely produced ctC145 mutant follicle-cell clones have
fewer, but larger, cells. This last phenotype agrees with our findings that
cut is required to maintain the follicle cells in mitotic cycle and
that ctdb7 mutation results in premature entry into the
endocycle. Study of the involvement of cut in this process required
generation of clones after the egg chamber exited the germarium, so that
defects caused by germarium requirements of cut would not interfere.
Interestingly, during both egg-chamber encapsulation and cell-cycle switch,
cut function was related to the Notch pathway. Cut expression was
downregulated by Notch signaling during the cell-cycle switch at stages 6-7.
In the germarium, cut negatively interacts with Notch, as
heterozygous cut mutation suppresses the Notch phenotype
(Jackson and Blochlinger,
1997
). Whether Cut acts as a target of Notch signaling at this
stage is unclear. We have studied gain- or loss-of-function clones of
Notch prior to stage 6 and detected no obvious change of Cut
expression (data not shown), which argues that Cut is not a downstream target
of Notch during early oogenesis.
|
|
The role of Cut in cell differentiation and cell cycle progression
The known role of Cut in Drosophila is mostly related to cell
differentiation. During neurogenesis, Cut is involved in cell-fate
determination in sensory-organ cells. Loss of cut function causes
transformation of the external sensory organ into the chordotonal sensory
organ, whereas overexpression of Cut has the opposite effect
(Merritt, 1997;
Blochlinger et al., 1991
). In
main-body follicle cells, we have shown that overexpression of Cut maintained
expression of immature cell-fate markers FasIII and Eya, whereas loss of
cut function in early stages repressed their expression. Although Cut
is involved in cell differentiation in these two developmental processes, its
roles in the two are significantly different. In sensory organs, the role of
Cut is post-mitotic, whereas in main-body follicle-cell differentiation, it
appears to be correlated with Cut function in the mitotic cycle. The
requirement for Cut in main-body follicle-cell differentiation may be related
to its function in cell-cycle regulation.
The role of cut in polar-cell differentiation is intriguing. Cut expression is normally retained in these specialized cells while its expression in main-body cells is decreased. We have shown that consistent expression of Cut led follicle cells to take the immature main-body cell fate, but these cells eventually took the polar-cell fate (Fig. 5G). Main-body cell fate and polar/stalk-cell fate are separated in the germarium, which requires Notch activity. Continuous Cut activity seemed able to reverse this differentiation process.
In contrast to the role of Drosophila Cut in cell differentiation,
mammalian Cut has mainly been shown to be involved in regulating cell-cycle
progression in some cell types (Coqueret
et al., 1998; Gupta et al.,
2003
; Truscott et al.,
2003
; Wu and Lee,
2002
). CDP, the mammalian homolog of Cut, has been shown to be
physically associated with the complex regulating the G1/S progression
(Coqueret et al., 1998
). Cut
could functionally replace E2F in forming a complex with RB in regulating
cell-cycle progression (Gupta et al.,
2003
). The requirement for Cut in maintaining the mitotic cell
cycle in Drosophila follicle cells echoes its role in mammalian
systems. Whether Drosophila E2F has a function in follicle cell
proliferation is not known; weak alleles of E2F1 and E2F2 affect gene
amplification, whereas no defect appears in the mitotic cycle
(Cayirlioglu et al., 2001
;
Cayirlioglu et al., 2003
;
Royzman et al., 1999
). Cut may
functionally replace E2F for cell-cycle progression in proliferating follicle
cells, but it is not an essential regulator of the cell cycle machinery
because the mitotic cycle did not seem to be affected in cut germline
clones (data not shown). In addition, cut function has been
extensively studied during embryogenesis and in imaginal discs, but no
reported function is related to cell-cycle regulation in these developmental
stages. The requirement for Cut in cell-cycle regulation is therefore probably
specific to follicle cells in Drosophila.
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ACKNOWLEDGMENTS |
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