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Notch-Dependent Downregulation of the Homeodomain Gene Cut Is Research article 4299 Notch-dependent downregulation of the homeodomain gene cut is required for the mitotic cycle/endocycle switch and cell differentiation in Drosophila follicle cells Jianjun Sun and Wu-Min Deng* Department of Biological Science, Florida State University, Tallahassee, FL 32306-4370, USA *Author for correspondence (e-mail: [email protected]) Accepted 28 July 2005 Development 132, 4299-4308 Published by The Company of Biologists 2005 doi:10.1242/dev.02015 Summary During Drosophila mid-oogenesis, follicular epithelial cells By contrast, prolonged expression of Cut caused defects in switch from the mitotic cycle to the specialized endocycle the mitotic cycle/endocycle switch. These cells continued to in which the M phase is skipped. The switch, along with express an essential mitotic cyclin, Cyclin A, which is cell differentiation in follicle cells, is induced by Notch normally degraded by the Fizzy-related-APC/C ubiquitin signaling. We show that the homeodomain gene cut proteosome system during the endocycle. Cut promoted functions as a linker between Notch and genes that are Cyclin A expression by negatively regulating Fizzy-related. involved in cell-cycle progression. Cut was expressed in Our data suggest that Cut functions in regulating both cell proliferating follicle cells but not in cells in the endocycle. differentiation and the cell cycle, and that downregulation Downregulation of Cut expression was controlled by the of Cut by Notch contributes to the mitotic cycle/endocycle Notch pathway and was essential for follicle cells to switch and cell differentiation in follicle cells. differentiate and to enter the endocycle properly. cut- mutant follicle cells entered the endocycle and Key words: cut, Endocycle, Cell cycle transition, Notch signaling, differentiated prematurely in a cell-autonomous manner. Drosophila melanogaster Development Introduction disc (Beatus and Lendahl, 1998; Bray, 1998). In oogenesis, The development of a multicellular organism requires Notch signaling has been shown to be implicated in the regulation of cellular behavior that is highly orchestrated specification of the polar follicle cells and regulation of cell- temporally and spatially. The coordination of cellular behavior cycle programs in the follicle-cell epithelium (Althauser et al., at the molecular level is made possible by mechanisms of cell- 2005; Deng et al., 2001; Grammont and Irvine, 2001; Lopez- cell signaling, which permit cells to influence each other’s fate Schier and St Johnston, 2001; Ruohola et al., 1991; Torres et and behavior. One of the most important mechanisms of cell al., 2003). signaling is mediated by Notch, a transmembrane receptor that Drosophila oogenesis is a highly regulated developmental coordinates a signaling system known as the Notch pathway, process [for a review of oogenesis, see Spradling (Spradling, which is evolutionarily conserved across metazoans and has a 1993)]. During oogenesis, the somatically derived follicle cells key role in cell-fate determination and pattern formation and the germline cells communicate with each other; disruption (Artavanis-Tsakonas et al., 1999; Bray, 1998; Greenwald, of the development of one invariably affects the other. This 1998; Schweisguth, 2004). The basic components of the tightly regulated mutual differentiation process serves as an pathway are the Notch receptor, DSL-type ligands, Delta (Dl) excellent model for the study of cell-cell communication and and Serrate (Delta and Jagged in vertebrates), and the temporal and spatial control of cell differentiation (Deng and transcription factor Suppressor of Hairless (Su(H); Bownes, 1998). During oogenesis, the main-body follicle cells CBF1/KBF2/RBP-Jk in mammals). Notch signals through a undergo three different modes of cell cycle as they develop. conserved and regulated intramembrane proteolysis (Mumm From the germarium to stage 6, these cells undergo an and Kopan, 2000; Selkoe and Kopan, 2003). Binding between archetypal mitotic cycle that includes complete G1, S, G2 and the extracellular domain of the receptor and the ligand activates M phases (Fig. 1A), during which the expression of mitotic the proteolysis and the release of the intracellular domain of markers, such as G2 cyclins, Cyclin A (CycA) and Cyclin B Notch (NICD), which is then shuttled into the nucleus and (CycB), and phosphohistone 3 (PH3), oscillates (Deng et al., converts the transcriptional repressor Su(H) into an activator. 2001; Schaeffer et al., 2004) (Fig. 1B). Beginning at around The Notch pathway has a wide range of biological roles in stage 7, main-body follicle cells undergo three rounds of Drosophila development. Notably, it is implicated in a lateral the endocycle (also called endoreplication or the inhibition process during neurogenesis that restricts sensory- endoreduplication cycle), which includes only the G and S organ formation and boundary formation in the wing imaginal phases (Edgar and Orr-Weaver, 2001; Lee and Orr-Weaver, 4300 Development 132 (19) Research article 2003) (Fig. 1A). As a result, 16 copies of genomic DNA are involved in cell-cycle progression in some cell types (Coqueret present in each nucleus. The switch from the mitotic cycle to et al., 1998). Here we show that, in Drosophila follicle cells, the endocycle is marked by abrupt disappearance of mitotic Cut also regulates the cell cycle, a function that may have been cyclins and PH3 (Bradbury, 1992; Deng et al., 2001; Hendzel conserved during evolution. et al., 1997). Endocycle cells retain oscillating patterns of Our data show that Cut expression is downregulated by the expression of Cyclin E (CycE) and genomic 5-bromo-2- Notch pathway in follicle cells during mid-oogenesis and that deoxyuridine (BrdU) incorporation (Follette et al., 1998). the downregulation is necessary for proper entry of follicle Coupled with the switch from the mitotic cycle to the cells into the endocycle and for their differentiation. In our endocycle, follicle cells show downregulation of immature- experiments, loss of cut function resulted in premature entry cell-fate markers such as Fasciclin III (FasIII); this into the endocycle and cell-autonomous differentiation. Cut downregulation could serve as a marker for follicle-cell promoted CycA expression by negatively regulating Fzr. Our differentiation (Lopez-Schier and St Johnston, 2001). At stage results suggest that Cut functions as a linker between Notch 10B, main-body follicle cells exit the endocycle and undergo and genes that are involved in cell-cycle progression and cell amplification of specific genomic regions (e.g. the chorion differentiation. 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). Materials and methods The switch from the mitotic cycle to the endocycle is Fly stocks induced by Notch signaling (Deng et al., 2001; Lopez-Schier 55e11 55e11 and St Johnston, 2001). At around stage 6 of oogenesis, Dl The following fly stocks were used: N FRT101 [N is an amorphic allele of Notch (N); a gift from Y. N. Jan]; FRT 82B Dl rev10 expression is elevated in the germline cells, coincident with the (Dlrev10 is an amorphic allele of Dl that is produced by excision of the transition from the mitotic cycle to the endocycle and promoter region, transcription start site, and first exon) (Heitzler and downregulation of FasIII. Indeed, removal of Dl function in the Simpson, 1991; Zeng et al., 1998); Su(H)SF8 FRT40A (Su(H)SF8 is a germline cells or Notch function in the follicle cells keeps strong loss-of-function allele of Su(H), a gift from S. Blair); follicle cells in the mitotic cycle during mid-oogenesis (stages psnC1FRT2A [psnC1 is a null mutant of psn (Struhl and Greenwald, 7 to 10A). In addition, the immature follicle-cell-fate marker, 1999)]; ctC145 FRT18A (Jackson and Blochlinger, 1997); ctdb7 [ctdb7 is FasIII, remains expressed at a high level in these cells. Notch- an amorphic allele of cut, has a 1 kb deletion in 130 to 150 kb, encodes dependent cell-cycle transition and cell differentiation require a protein lacking the homeodomain, and belongs to the lethal II cut protein cleavage, as ␥-secretase components Presenilin (Psn) phenotypic class (Brewster and Bodmer, 1995)] was recombined to and Nicastrin are involved in this process (Lopez-Schier and the FRT18D chromosome. To generate N55e11, Dlrev10, Su(H)SF8, St Johnston, 2001; Lopez-Schier and St Johnston, 2002). In psnC1, ctC145, and ctdb7 mutant clones, we used yw Ubi-GFP addition, the nuclear effector of Notch signaling, Su(H), is FRT101;MKRS P{ry=hsFLP}86E/TM6BTb, hsFLP;FRT82B Ubi- Development needed for the switch (Deng et al., 2001; Lopez-Schier and St GFP/TM3, hsFLP;GFP FRT40A/Cyo, GFP FRT2A, GFP FRT 18A; Johnston, 2001). Notch signaling negatively regulates String MKRS P{ry=hsFLP}86E/TM6B, and hGFP FRT18D;MKRS (Stg)/cdc25 phosphatase and G2 cyclins and positively P{ry=hsFLP}86E/TM6BTb, respectively. For analysis of the regulates Fizzy-related/Hec1/Cdh1 (Fzr) (Deng et al., 2001; overexpression phenotype, the following stocks were used: UAS- NICD UAS-cut Schaeffer et al., 2004; Shcherbata et al., 2004). Fzr, also known [an active form of Notch (Rauskolb et al., 1999)], (a gift from R. Bodmer), UAS-stgN16 (Reis and Edgar, 2004) and hsFLP; as Retina aberrant in pattern, is a conserved WD domain act<CD2<Gal4, UAS-GFP/TM3. The fzr-lacZ line (fzrG0326, a protein. Previous studies have shown that Fzr is required for P{lacW} element inserted in the first intron of the Fizzy-related gene) degeneration of G2 cyclins in an anaphase promoting (Peter et al., 2002) and stg-lacZ line [pstg␤-R6.4 (Deng et al., 2001; complex/cyclosome (APC/C) E3 ligase-dependent manner. Lehman et al., 1999)] were used to detect the fzr and stg expression Loss of fzr function in Drosophila follicle cells causes defects in the Cut-overexpressing follicle-cell clones, respectively. A101/TM3 in the mitotic-to-endocycle transition and results in the (neuralized-lacZ) and PZ80/Cyo were also used as the polar-cell-fate maintenance of CycA expression after stage 6 during oogenesis marker (Larkin et al., 1996; Adam and Montell, 2004).
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