Tissue remodeling: a mating-induced differentiation program for the Drosophilaoviduct

Anat Kapelnikov,Ronald R Hoy,Patricia K Rivlin,Yael Heifetz

doi:10.1186/1471-213x-8-114

Anat Kapelnikov, Ronald R Hoy + Show 2 more

Open Access

https://doi.org/10.1186/1471-213x-8-114

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Abstract

BackgroundIn both vertebrates and invertebrates, the oviduct is an epithelial tube surrounded by visceral muscles that serves as a conduit for gamete transport between the ovary and uterus. While Drosophila is a model system for tubular organ development, few studies have addressed the development of the fly's oviduct. Recent studies in Drosophila have identified mating-responsive genes and proteins whose levels in the oviduct are altered by mating. Since many of these molecules (e.g. Muscle LIM protein 84B, Coracle, Neuroglian) have known roles in the differentiation of muscle and epithelia of other organs, mating may trigger similar differentiation events in the oviduct. This led us to hypothesize that mating mediates the last stages of oviduct differentiation in which organ-specific specializations arise.ResultsUsing electron- and confocal-microscopy we identified tissue-wide post-mating changes in the oviduct including differentiation of cellular junctions, remodeling of extracellular matrix, increased myofibril formation, and increased innervation. Analysis of once- and twice-mated females reveals that some mating-responsive proteins respond only to the first mating, while others respond to both matings.ConclusionWe uncovered ultrastructural changes in the mated oviduct that are consistent with the roles that mating-responsive proteins play in muscle and epithelial differentiation elsewhere. This suggests that mating triggers the late differentiation of the oviduct. Furthermore, we suggest that mating-responsive proteins that respond only to the first mating are involved in the final maturation of the oviduct while proteins that remain responsive to later matings are also involved in maintenance and ongoing function of the oviduct. Taken together, our results establish the oviduct as an attractive system to address mechanisms that regulate the late stages of differentiation and maintenance of a tubular organ.

Highlights

In both vertebrates and invertebrates, the oviduct is an epithelial tube surrounded by visceral muscles that serves as a conduit for gamete transport between the ovary and uterus
In most mated reproductive tracts processed for microscopy (8/9), an egg was located in one of the lateral oviducts, whereas an egg was never observed in the oviduct of unmated reproductive tracts (5/5) (Figure 1)
Initial formation of cell-cell junctions in oviduct epithelia is mating-independent To determine whether mating induces specific morphological changes in the oviduct epithelia post-mating, we examined the ultrastructure of the oviduct epithelia in unmated and mated reproductive tracts

Summary

Introduction

In both vertebrates and invertebrates, the oviduct is an epithelial tube surrounded by visceral muscles that serves as a conduit for gamete transport between the ovary and uterus. In Drosophila, the best understood tubular organs from a developmental point of view are the trachea and salivary gland Studies of these organs reveal a general program for tubular organ development, in which combinatorial expression of global patterning genes specifies positions within the embryo for the subsequent activation of tissue-specific early genes and transcription factors. This program results in the activation of downstream genes involved in terminal differentiation of organ-specific specializations such as the cuticle that lines the tracheal lumen [1,2,4,7,8,9]

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