Abstract
The study of the telomeric complex in oogenesis and early development is important for understanding the mechanisms which maintain genome integrity. Telomeric transcripts are the key components of the telomeric complex and are essential for regulation of telomere function. We study the biogenesis of transcripts generated by the major Drosophila telomere repeat HeT-A in oogenesis and early development with disrupted telomeric repeat silencing. In wild type ovaries, HeT-A expression is downregulated by the Piwi-interacting RNAs (piRNAs). By repressing piRNA pathway, we show that overexpressed HeT-A transcripts interact with their product, RNA-binding protein Gag-HeT-A, forming ribonucleoprotein particles (RNPs) during oogenesis and early embryonic development. Moreover, during early stages of oogenesis, in the nuclei of dividing cystoblasts, HeT-A RNP form spherical structures, which supposedly represent the retrotransposition complexes participating in telomere elongation. During the later stages of oogenesis, abundant HeT-A RNP are detected in the cytoplasm and nuclei of the nurse cells, as well as in the cytoplasm of the oocyte. Further on, we demonstrate that HeT-A products co-localize with the transporter protein Egalitarian (Egl) both in wild type ovaries and upon piRNA loss. This finding suggests a role of Egl in the transportation of the HeT-A RNP to the oocyte using a dynein motor. Following germline piRNA depletion, abundant maternal HeT-A RNP interacts with Egl resulting in ectopic accumulation of Egl close to the centrosomes during the syncytial stage of embryogenesis. Given the essential role of Egl in the proper localization of numerous patterning mRNAs, we suggest that its abnormal localization likely leads to impaired embryonic axis specification typical for piRNA pathway mutants.
Highlights
Telomeres are DNA-protein complexes that protect the ends of linear eukaryotic chromosomes
To get an insight into the biogenesis and pathological significance of abundant telomeric RNAs and proteins generated upon telomere dysfunction, we characterized their localization during oogenesis and first hours of development after germline knockdown (GLKD) of spnE
We proposed that in the wild type ovaries, HeT-A ribonucleoprotein particles (RNPs) interact with Egl and performed Egl and HeT-A Gag immunostaining combined with HeT-A RNA fluorescence in situ hybridization (FISH) on ovaries of the Gaiano III (GIII) strain, which is characterized by an increased HeT-A copy number [25]
Summary
Telomeres are DNA-protein complexes that protect the ends of linear eukaryotic chromosomes. In most species telomeric repeats are synthesized by telomerase consisting of reverse transcriptase and an RNA template. Telomere-associated proteins form the telomere protection shelterin complex [1]. It was found that telomeric repeats are transcribed and give rise to long non-coding RNAs, TERRA [2]. TERRA molecules interact with shelterin proteins, telomerase, chromatin remodeling factors and localize near telomeres suggesting a structural role in telomere architecture [3]. TERRA may bind and regulate different genic targets indicating its role as an epigenetic factor in gene expression [4]. The large network of TERRA interacting proteins suggests that TERRA plays a significant role in telomere regulation and in various cellular pathways [4, 5]. The functional significance of most interactions between TERRA and its partners remains poorly understood
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