Abstract
Follicle rupture, the final step in ovulation, utilizes conserved molecular mechanisms including matrix metalloproteinases (Mmps), steroid signaling, and adrenergic signaling. It is still unknown how follicles become competent for follicle rupture/ovulation. Here, we identify a zinc-finger transcription factor Hindsight (Hnt) as the first transcription factor regulating follicle's competency for ovulation in Drosophila. Hnt is not expressed in immature stage-13 follicle cells but is upregulated in mature stage-14 follicle cells, which is essential for follicle rupture/ovulation. Hnt upregulates Mmp2 expression in posterior follicle cells (essential for the breakdown of the follicle wall) and Oamb expression in all follicle cells (the receptor for receiving adrenergic signaling and inducing Mmp2 activation). Hnt's role in regulating Mmp2 and Oamb can be replaced by its human homolog Ras-responsive element-binding protein 1 (RREB-1). Our data suggest that Hnt/RREB-1 plays conserved role in regulating follicle maturation and competency for ovulation.
Highlights
Ovulation is a complex process of releasing fertilizable oocytes from mature follicles and is essential for animal reproduction (Espey and Richards, 2006)
By using molecular and genetic tools, we demonstrated that Hnt expression in stage-14 follicle cells is essential for follicle rupture partly by upregulation of Oamb and Matrix metalloproteinase 2 (Mmp2) expression in these follicle cells
To determine the developmental sequence of the aforementioned three types of stage-14 egg chambers, we analyzed the expression patterns of Hnt against the expression of a stage-14 follicle-cell Gal4 driver (44E10-Gal4; renamed as FC1 for simplicity) (Deady and Sun, 2015) and the number of nurse cell nuclei in these egg chambers. 86% of A/P-Hnt egg chambers had medium-level GFP expression driven by FC1, while more than 73% of high-Hnt and 80% of low-Hnt egg chambers had high-level GFP expression (Figure 2A–D)
Summary
Ovulation is a complex process of releasing fertilizable oocytes from mature follicles and is essential for animal reproduction (Espey and Richards, 2006). Several proteolytic systems have been found to regulate follicle rupture in vertebrates, including matrix metalloproteinase (Mmp), plasminogen activator/plasmin, and ADAMS-TS (Curry and Smith, 2006; Takahashi et al, 2013). Molecular mechanisms coupling the Ras-MAPK pathway to the activation of proteolytic systems for follicle rupture are largely unknown. Ovulation in Drosophila utilizes conserved molecular mechanisms and involves a follicle rupture process to release mature oocytes from the ovary. Each ovary contains ~16 ovarioles, where egg chambers are assembled in the germarium at the anterior and develop through 14 characteristic stages toward the posterior end (Spradling, 1993). In stage-14 egg chambers ( named mature follicles), all nurse cells are degraded, leaving an oocyte surrounded by follicle cells; Matrix metalloproteinase 2 (Mmp2) is upregulated in posterior follicle cells (Figure 1; Deady et al, 2015). Oamb (octopamine receptor in mushroom body), encoding an a-adrenergic receptor-like G-protein-coupled receptor for octopamine (OA), is upregulated in all follicle cells of stage-14
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