Arginine methylation of SmB is required for Drosophila germ cell development

Abstract

SUMMARYSm proteins constitute the common core of spliceosomal small nuclear ribonucleoproteins. Although Sm proteins are known to be methylated at specific arginine residues within the C-terminal arginine-glycine dipeptide (RG) repeats, the biological relevance of these modifications remains unknown. In this study, a tissue-specific function of arginine methylation of the SmB protein was identified in Drosophila. Analysis of the distribution of SmB during oogenesis revealed that this protein accumulates at the posterior pole of the oocyte, a cytoplasmic region containing the polar granules, which are necessary for the formation of primordial germ cells. The pole plasm localisation of SmB requires the methylation of arginine residues in its RG repeats by the Capsuléen-Valois methylosome complex. Functional studies showed that the methylation of these arginine residues is essential for distinct processes of the germline life cycle, including germ cell formation, migration and differentiation. In particular, the methylation of a subset of these arginine residues appears essential for the anchoring of the polar granules at the posterior cortex of the oocyte, whereas the methylation of another subset controls germ cell migration during embryogenesis. These results demonstrate a crucial role of arginine methylation in directing the subcellular localisation of SmB and that this modification contributes specifically to the establishment and development of germ cells.

PRMT5 and the role of symmetrical dimethylarginine in chromatoid bodies of planarian stem cells

“…Functional analyses have shown that the PRMT5/PIWI/TUDOR network plays a role in the piRNA processing pathway, retrotransposon silencing and, consequently, genomic stability (Nishida et al, 2009;Reuter et al, 2009;Shoji et al, 2009;reviewed by Siomi et al, 2011). By contrast, the PRMT5/Sm/TUDOR network present in fly oocytes is involved in localization of oskar mRNA and specification of germ cell fate (Anne et al, 2007;Anne, 2010;Boswell and Mahowald, 1985;Gonsalvez et al, 2006;Gonsalvez et al, 2010). Our biochemical and sequence analyses suggest that both SMEDWI-3 and Sm protein family members are methylated in planarians.…”

“…Y12 specifically recognizes sDMA (Brahms et al, 2000), suggesting that neoblasts express machinery necessary for this modification. Recent reports have shown that interactions between proteins containing sDMA and TDRDs are important for RNP aggregation in mouse and fly germlines (Anne, 2010;Gonsalvez et al, 2010;Kirino et al, 2010b;Vagin et al, 2009b). Given that neoblasts are enriched with expression of tudor homologs Yoshida-Kashikawa et al, 2007) and that one homolog is a neoblast CB component (Solana et al, 2009), we analyzed sDMAcontaining proteins in neoblasts.…”

Functional interplay between protein arginine methyltransferases in Trypanosoma brucei

“…In higher eukaryotes, PRMTs can regulate cell development and differentiation. For example, in Drosophila , arginine methylation by their PRMTs (DARTS) has been linked to establishment of germ cells and wing development (Anne ; Xu et al. ).…”

RIP-seq analysis of eukaryotic Sm proteins identifies three major categories of Sm-containing ribonucleoproteins

“…In Caenorhabditis elegans , Sm proteins, but not other splicing factors, localize to germline P granules and are required for their integrity [19,20]. In Drosophila melanogaster , SmB and SmD3 are enriched at the posterior pole of developing oocytes [21,22], and a hypomorphic mutation in SmD3 causes mislocalization of oskar mRNPs and pronounced defects in germ cell specification that are independent from splicing [21]. Moreover, loss of the Sm protein methyltransferase PRMT5 results in failure to specify the germline [21,23,24].…”