MiR-989 Is Required for Border Cell Migration in the Drosophila Ovary

Jan-Michael Kugler,Ya-Wen Chen,Stephen M Cohen,Ruifen Weng

doi:10.1371/journal.pone.0067075

Jan-Michael Kugler, Ya-Wen Chen + Show 2 more

Open Access

https://doi.org/10.1371/journal.pone.0067075

Copy DOI

Abstract

microRNAs (miRNAs) are small non-coding RNAs that regulate gene expression by destabilizing target transcripts and/or inhibiting their translation. miRNAs are thought to have roles in buffering gene expression to confer robustness. miRNAs have been shown to play important roles during tissue development to control cell proliferation, differentiation and morphogenesis. Many miRNAs are expressed in the germ line of Drosophila, and functions have been reported for a few miRNAs in maintenance of stem cell proliferation during oogenesis. Here, we analyse the function of Drosophila miR-989 in oogenesis. miR-989 is abundant in ovaries. Mutants lacking miR-989 did not display gross abnormalities affecting egg chamber formation or maturation. However, the migration of the border cell cluster was severely delayed in miR-989 mutant egg chambers. We demonstrate that miR-989 function is required in the somatic cells in the egg chamber, not in germ line cells for border cell migration. Loss of miR-989 from a fraction of the border cell cluster was sufficient to impair cluster migration as a whole, suggesting a role in border cells. Gene ontology analysis reveals that many predicted miR-989 target mRNAs are implicated in regulating cell migration, cell projection morphogenesis, cell adhesion as well as receptor tyrosine kinase and ecdysone signalling, consistent with an important regulatory role for miR-989 in border cell migration.

Highlights

MiRNAs are small non-coding RNAs that function as regulators of gene expression in a wide range of biological contexts [1,2]. miRNAs associate with their target transcripts via partial complementary base pairing to target sites which are usually located in the target 3’UTR or in coding sequences [3,4]
Drosophila eggs mature in compound entities called egg chambers, which are comprised of 16 interconnected germ-line cells that are encapsulated by a monolayer of somatic follicle cells [8] (Fig. 1)
Delayed border cell migration We observed that border cell migration was frequently delayed in miR-989KO / Df(2R)Exel7130 ovaries compared to controls and quantitated this phenotype during two stages of egg chamber development (Fig 2)

Summary

Introduction

MiRNAs are small non-coding RNAs that function as regulators of gene expression in a wide range of biological contexts [1,2]. miRNAs associate with their target transcripts via partial complementary base pairing to target sites which are usually located in the target 3’UTR or in coding sequences [3,4]. We show that border cell migration is delayed in miR-989 mutant egg chambers, and that this phenotype can be rescued by transgenic expression of the miRNA. We demonstrate that miR-989 is active in the somatic cells of the egg chamber and required in border cells for efficient migration.

Results

Conclusion