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

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.

Somatic piRNAs and Transposons are Differentially Expressed Coincident with Skeletal Muscle Atrophy and Programmed Cell Death

“…For example, in Drosophila , the piRNA pathway proteins Aub and Ago3 regulate transposon expression and mobilization in the mushroom bodies, brain structures that regulate memory formation and cognitive function ( Perrat et al, 2013 ). These proteins are also found in specialized structures within glial cells in the adult Drosophila brain where they appear to repress transposon activity ( Tindell et al, 2020 ). In the sea slug Aplysia , a specific piRNA has been shown to modulate synaptic plasticity and memory ( Lee et al, 2011 ; Rajasethupathy et al, 2012 ).…”

Looking at the Pretty “Phase” of Membraneless Organelles: A View From Drosophila Glia

“…Since one of the principal components of the Drosophila germ granules, Tud scaffold protein (Arkov et al, 2006;Gao et al, 2015;Vo et al, 2019), was found to be expressed not only in germline but also in the Drosophila head, distribution of Tud in the adult brain was recently examined in more detail (Tindell et al, 2020). These experiments led to the identification of Tud-containing large granules of about 0.5-2 μm in size in the cytoplasm of specific types of glial cells (but not in the neurons of the adult brain) (Tindell et al, 2020), Figure 1).…”

“…In this mini review, the author highlights novel membraneless granules identified in glia of the adult Drosophila brain (referred to as "glial granules") (Tindell et al, 2020), which were found to contain protein components of germ granules and discuss the potential significance of glial granules for brain functions in the context of other membraneless organelles.…”

Somatic piRNAs and Transposons are Differentially Regulated During Skeletal Muscle Atrophy and Programmed Cell Death

“…For example, in Drosophila, the piRNA pathway proteins Aub and Ago-3 regulate transposon expression and mobilization in the mushroom bodies, brain structures that regulate memory formation and cognitive function (33). These proteins are also found in specialized structures within glial cells in the adult Drosophila brain where they appear to repress transposon activity (34). In the sea slug Aplysia, a specific piRNA has been shown to modulate synaptic plasticity and memory (35, 36).…”