Abstract
DDX3 subfamily DEAD-box RNA helicases are essential developmental regulators of RNA metabolism in eukaryotes. belle, the single DDX3 ortholog in Drosophila, is required for fly viability, fertility, and germline stem cell maintenance. Belle is involved both in translational activation and repression of target mRNAs in different tissues; however, direct targets of Belle in the testes are essentially unknown. Here we showed that belle RNAi knockdown in testis cyst cells caused a disruption of adhesion between germ and cyst cells and generation of tumor-like clusters of stem-like germ cells. Ectopic expression of β-integrin in cyst cells rescued early stages of spermatogenesis in belle knockdown testes, indicating that integrin adhesion complexes are required for the interaction between somatic and germ cells in a cyst. To address Belle functions in spermatogenesis in detail we performed cross-linking immunoprecipitation and sequencing (CLIP-seq) analysis and identified multiple mRNAs that interacted with Belle in the testes. The set of Belle targets includes transcripts of proteins that are essential for preventing the tumor-like clusters of germ cells and for sustaining spermatogenesis. By our hypothesis, failures in the translation of a number of mRNA targets additively contribute to developmental defects observed in the testes with belle knockdowns both in cyst cells and in the germline.
Highlights
DEAD-box RNA helicases are important developmental regulators of gene expression
We found that ectopic expression of β-integrin in cyst cells rescued the differentiation of early germ cells in the bel knockdown (belKD) testes, indicating the importance of integrin adhesion complexes in the tight interaction between somatic cyst cells and germ cells in the cyst
We have shown that RNA helicase Belle (DDX3) is a critical cell-autonomous factor for survival and divisions of germline stem cells (GSCs) and spermatogonial cells in the Drosophila testes [25]
Summary
DEAD-box RNA helicases are important developmental regulators of gene expression. They operate by remodeling the local secondary structure of RNAs and RNA-protein complexes in an ATP-dependent manner to provide subsequent association of RNA-binding proteins to their RNA targets. This implicates a crucial role of DEAD-box RNA proteins in regulating ribonucleoprotein (RNP) complexes. DEAD-box RNA helicases participate in practically every stage of RNA metabolism, including transcription, processing, translation, ribosome biogenesis, splicing, RNA localization, RNA decay, and turnover [1,2,3].
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