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

Abstract

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.

High-Throughput Sequencing Reveals Differential Expression of miRNAs in Intestine from Sea Cucumber during Aestivation

“…Significant up-regulation of miR-92 was also detected in the intestine of deep aestivating sea cucumbers, which suggests that this miRNA may act to arrest the apoptotic response and help to maintain homeostasis under energy limited conditions like aestivation. Recently, miR-7 has been shown to have functional roles in the differentiation of intestinal epithelial cells [38] and plays an important role in developmental decision-making in association with signal-transduction pathways [39]. Sea cucumber intestine also showed a significant increase in miR-7 expression levels during aestivation and could be involved in the suppression of growth and proliferation in response to global metabolic rate depression during torpor.…”

P-bodies and the miRNA pathway regulate translational repression ofbicoidmRNA duringDrosophila melanogasteroogenesis

“…MiRNA gene mutants have been lacking in D. melanogaster, however a recent study from the Stephen Cohen group (12), which generated several dozen targeted miRNA knock-outs, will enable further studies of the functions of individual miRNAs during fly development. To date, several publications have demonstrated roles for specific miRNAs in various aspects of egg chamber patterning and early embryonic development (13)(14)(15). For example, miR-184 acts during egg chamber development to regulate stem cell differentiation, dorsal appendage patterning, and pair rule gene activation during embryogenesis (16), and miR-318 regulates follicle cell gene amplification and chorion formation (17).…”

Regulation of Pattern Formation and Gene Amplification During Drosophila Oogenesis by the miR-318 microRNA

“…A recent report has found that miR-7 miRNA regulates Ttk69 during the transition from endocycles to gene amplification. miR-7 overexpression was able to repress Ttk69 expression and delay the switch from endocycles to amplification, but loss of miR-7 was not sufficient to advance this process (Huang et al 2013).…”

“…expression of another transcription factor, Hindsight (Hnt), shows the opposite pattern, being higher during the endocycles and decreasing at stage 10B (Sun and Deng 2007). Increased Cut expression and decreased Hnt expression provide markers for the transition from endocycles to gene amplification (Huang et al 2013). We compared the expression patterns of Cut and Hnt in mutant and wild-type clones in stage 10B egg chambers.…”

“…miR-7 and miR-278 target Dacapo (Dap) to regulate cell cycle progression in germline stem cells (Yu et al 2009). miR-7 also regulates Tramtrack69 (Ttk69) to control a developmental switch in the follicle cells (Huang et al 2013). miR-279 represses signal transducer and activator of transcription (STAT) in both the follicle cells and migratory border cells to control cell fate (Yoon et al 2011).…”