Glial granules contain germline proteins in the Drosophila brain, which regulate brain transcriptome

Samuel J Tindell,Alexey L Arkov,Eric C Rouchka

doi:10.1038/s42003-020-01432-z

Samuel J Tindell, Alexey L Arkov + Show 1 more

Open Access

https://doi.org/10.1038/s42003-020-01432-z

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Abstract

Membraneless RNA-protein granules play important roles in many different cell types and organisms. In particular, granules found in germ cells have been used as a paradigm to study large and dynamic granules. These germ granules contain RNA and proteins required for germline development. Here, we unexpectedly identify large granules in specific subtypes of glial cells (“glial granules”) of the adult Drosophila brain which contain polypeptides with previously characterized roles in germ cells including scaffold Tudor, Vasa, Polar granule component and Piwi family proteins. Interestingly, our super-resolution microscopy analysis shows that in the glial granules, these proteins form distinct partially overlapping clusters. Furthermore, we show that glial granule scaffold protein Tudor functions in silencing of transposable elements and in small regulatory piRNA biogenesis. Remarkably, our data indicate that the adult brain contains a small population of cells, which express both neuroblast and germ cell proteins. These distinct cells are evolutionarily conserved and expand during aging suggesting the existence of age-dependent signaling. Our work uncovers previously unknown glial granules and indicates the involvement of their components in the regulation of brain transcriptome.

Highlights

Membraneless RNA-protein granules play important roles in many different cell types and organisms
Immunostaining of the whole-mount brains with anti-green fluorescent protein (GFP) and anti-FLAG antibodies to detect Tud and different brain markers indicated that Tud is expressed in the brain glia labeled with antibody against Reversed polarity (Repo) protein, which is a specific marker for all types of glial cells (Fig. 1a)
In this study, using super-resolution microscopy, we identified, to the best of our knowledge, new structures in glia of the Drosophila adult brain (“glial granules”), which contain germ granule proteins required for germline development including Tud, Vas, polar granule components (Pgcs), Ago[3], and Piwi

Summary

Introduction

Membraneless RNA-protein granules play important roles in many different cell types and organisms. Granules found in germ cells have been used as a paradigm to study large and dynamic granules These germ granules contain RNA and proteins required for germline development. We unexpectedly identify large granules in specific subtypes of glial cells (“glial granules”) of the adult Drosophila brain which contain polypeptides with previously characterized roles in germ cells including scaffold Tudor, Vasa, Polar granule component and Piwi family proteins. We show that Tud and other germ cell proteins, previously studied for their unique roles in the germline, are expressed in the adult brain, and overall, these germ cell polypeptides assemble in large granules in glia (here referred to as glial granules), contribute to the genome integrity and regulate brain transcriptome. Our study indicates the roles of genes in the adult brain whose functions have been traditionally viewed as being specific to germ cells

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