The microRNA pathway regulates the temporal pattern of Notch signaling in <i>Drosophila</i> follicle cells

Poulton, Joanna; Huang, Yi-Chun; Smith, Laila; Sun, Jianjun; Leake, Nicholas; Schleede, Justin; Stevens, Leslie M.; Deng, Wu-Min

doi:10.1242/jcs.091264

Cited by 9 publications

(14 citation statements)

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“…It has been shown that cyst growth is induced by neural-derived insulin-like peptides (LaFever and Drummond-Barbosa, 2005), but it is unknown how proliferation in the epithelium is controlled. Cell divisions cease after stage 6 of oogenesis in a process mediated by activation of Notch signalling in epithelial cells, which is again induced by Delta expression in the germline (Deng et al, 2001;López-Schier and St Johnston, 2001;Poulton et al, 2011). Subsequently, epithelial morphogenesis starts with the formation of a squamous anterior and a columnar posterior epithelium.…”

Section: Introductionmentioning

confidence: 99%

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

Berns¹,

Woichansky²,

Friedrichsen³

et al. 2014

Development

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The Drosophila oogenesis system provides an excellent model to study the development of epithelial tissues. Here, we report the first genome-scale in vivo RNA interference (RNAi) screen for genes controlling epithelial development. By directly analysing cell and tissue architecture we identified 1125 genes, which we assigned to seven different functions in epithelial formation and homeostasis. We validated the significance of our screen by generating mutants for Vps60, a component of the endosomal sorting complexes required for transport (ESCRT) machinery. This analysis provided new insights into spatiotemporal control of cell proliferation in the follicular epithelium. Previous studies have identified signals controlling divisions in the follicle stem cell niche. However, 99% of cell divisions occur outside of the niche and it is unclear how these divisions are controlled. Our data distinguish two new domains outside of the stem cell niche where there are differing controls on proliferation. One domain abuts the niche and is characterised by ESCRT, Notch and JAK/STAT-mediated control of proliferation. Adjacent to this domain, another domain is defined by loss of the impact of ESCRT on cell division. Thus, during development epithelial cells pass through a variety of microenvironments that exert different modes of proliferation control. The switch between these modes might reflect a decrease in the 'stemness' of epithelial cells over time.

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Section: Introductionmentioning

confidence: 99%

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

Berns¹,

Woichansky²,

Friedrichsen³

et al. 2014

Development

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“…The rise and fall (activation and downregulation) of Notch signaling in the follicle cells have direct effects on the two developmental switches. miRNAs, however, play important modulatory roles in controlling the timing of these two switches (Poulton et al, 2011; this study), but clear differences exist. During the mitotic-to-endocycle switch, the miRNAs directly regulate the 903 RESEARCH ARTICLE miR-7 in a developmental switch Δ1 MARCM clones (outlined and marked by RFP, red) with ttk69-RNAi expression in this stage 11 egg chamber (top, sectional views; bottom, surface views).…”

Section: Discussionmentioning

confidence: 75%

“…Similarly, their homologs in Drosophila (miR-125 and let-7) are involved in temporal regulation of metamorphic processes (Caygill and Johnston, 2008;Sokol et al, 2008), suggesting a conserved role for these miRNAs in temporal regulation of development. Our recent study revealed the miRNA biogenesis pathway functions in the transition from the mitotic cycle to the endocycle in the follicle cells of the fly egg chamber (Poulton et al, 2011). Here, we report that miR-7 modulates the E/A switch by acting directly on Ttk69 transcripts.…”

Section: Introductionmentioning

confidence: 73%

“…Overexpression of miR-7 leads to a failure to switch to the gene amplification stage Previously, we have reported that the miRNA biogenesis pathway, including Dicer-1 and Pasha is involved in regulation of the temporal pattern of Notch signaling and the cell-cycle switches in the follicular epithelium (Poulton et al, 2011). To identify the miRNA(s) involved in this regulation, we looked at miR-7, which has been reported to regulate Notch and EGFR pathways in Drosophila imaginal discs and sensory organ precursors (Li et al, 2009).…”

Section: Resultsmentioning

confidence: 99%

“…Scale bars: 10 µm. timing of Notch activation by acting on cis-expressed Delta (Poulton et al, 2011). During the E/A switch, the miRNA miR-7, does not seem to have a direct role in regulating Notch activity; instead, it acts directly on the transcription factor Ttk69, which is also a target of Notch and EcR signaling in this process.…”

Section: Discussionmentioning

confidence: 99%

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The microRNA miR-7 regulates Tramtrack69 in a developmental switch in Drosophila follicle cells

et al. 2013

Self Cite

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SUMMARYDevelopment in multicellular organisms includes both small incremental changes and major switches of cell differentiation and proliferation status. During Drosophila oogenesis, the follicular epithelial cells undergo two major developmental switches that cause global changes in the cell-cycle program. One, the switch from the endoreplication cycle to a gene-amplification phase, during which special genomic regions undergo repeated site-specific replication, is attributed to Notch downregulation, ecdysone signaling activation and upregulation of the zinc-finger protein Tramtrack69 (Ttk69). Here, we report that the microRNA miR-7 exerts an additional layer of regulation in this developmental switch by regulating Ttk69 transcripts. miR-7 recognizes the 3′ UTR of ttk69 transcripts and regulates Ttk69 expression in a dose-dependent manner. Overexpression of miR-7 effectively blocks the switch from the endocycle to gene amplification through its regulation of ttk69. miR-7 and Ttk69 also coordinate other cell differentiation events, such as vitelline membrane protein expression, that lead to the formation of the mature egg. Our studies reveal the important role miR-7 plays in developmental decision-making in association with signal-transduction pathways.

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Modulation of cell morphogenesis by tousled‐like kinase in the Drosophila follicle cell

Yeh¹,

Huang²,

Lan³

et al. 2015

Developmental Dynamics

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Background: Tousled-like kinase (Tlk) is a conserved serine/threonine kinase regulating DNA replication, chromatin assembly, and DNA repair. Previous studies have suggested that Tlk is involved in cell morphogenesis in vitro. In addition, tlk genetically interact with Rho1, which encodes a key regulator of the cytoskeleton. However, whether Tlk plays a physiological role in cell morphogenesis and cytoskeleton rearrangement remains unknown. Results: In tlk mutant follicle cells, area of the apical domain was reduced. The density of microtubules was increased in tlk mutant cells. The density of actin filaments was increased in the apical region and decreased in the basal region. Because area of the apical domain was reduced, we examined the levels of proteins located in the apical region by using immunofluorescence. The fluorescence intensities of two adherens junction proteins Armadillo (Arm) and DE-cadherin (DE-cad), atypical protein kinase C (aPKC), and Notch, were all increased in tlk mutant cells. The basolateral localized Discs large (Dlg) shifted apically in tlk mutant cells. Conclusions: Increase of protein densities in the apical region might be resulted from disruption of the cytoskeleton and shrinkage of the apical domain. Together, these data suggest a novel role of Tlk in maintaining cell morphology, possibly through modulating the cytoskeleton. Developmental Dynamics 244:852-865, 2015. V C 2015 Wiley Periodicals, Inc.

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The microRNA pathway regulates the temporal pattern of Notch signaling in Drosophila follicle cells

Cited by 9 publications

References 1 publication

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

A genome-scale in vivo RNAi analysis of epithelial development in Drosophila identifies new proliferation domains outside of the stem cell niche

The microRNA miR-7 regulates Tramtrack69 in a developmental switch in Drosophila follicle cells

Modulation of cell morphogenesis by tousled‐like kinase in the Drosophila follicle cell

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