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Germ cell division and encapsulation by somatic cells during Drosophila oogenesis require the orphan nuclear receptor ftz-f1

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posted on 20.04.2020 by Allison N. Beachum, Elizabeth Tweedie Ables

Gamete production in mammals and insects is controlled by cell signaling pathways that facilitate communication between germ cells and somatic cells. Nuclear receptor signaling is a key mediator of many aspects of reproduction, including gametogenesis. For example, the NR5A sub-family of nuclear receptors are essential for gonadogenesis and sex steroid production in mammals. Yet despite the original identification of the NR5A sub-family in the model insect Drosophila melanogaster, it has been unclear whether Drosophila NR5A receptors directly control oocyte production. Here, we demonstrate that ftz-f1 (NR5A3) is necessary for multiple aspects of early oocyte development. Ftz-f1 is expressed throughout the ovary, including in germline stem cells (GSCs), germline cysts, and several populations of somatic cells. Ftz-f1 is necessary in GSCs and their dividing daughters for timely mitotic cyst divisions and accumulation of oocyte-specific proteins in the presumptive oocyte which dictate oocyte positioning within the cyst. In parallel, ftz-f1 in somatic escort cells and pre-follicle cells promotes proper cyst division and cyst encapsulation. Interestingly, our data suggest that ftz-f1 promotes escort cell-dependent cyst encapsulation via a complex genetic interaction with the steroid hormone ecdysone. We propose the model that Ftz-f1 and ecdysone signaling via the Ecdysone Receptor (NR1H1) interdependently promote communication between escort cells and germ cells. Taken together, these results demonstrate that the reproductive functions of the NR5A sub-family are largely conserved between insects and mammals. Our data underscore the importance of nuclear receptors in the control of reproduction and highlight the utility of Drosophila oogenesis as a key model for unraveling the complexity of nuclear receptor signaling in gametogenesis.

Funding

National Institutes of Health R15 GM117502

East Carolina University Division of Research and Graduate Studies

East Carolina University Thomas Harriot College of Arts and Sciences

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1604B

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