Temporal complexity within a translational control element in thenanosmRNA

Abstract

Translational control of gene expression plays a fundamental role in the early development of many organisms. In Drosophila, selective translation of nanos mRNA localized to the germ plasm at the posterior of the embryo, together with translational repression of nanos in the bulk cytoplasm, is essential for development of the anteroposterior body pattern. We show that both components to spatial control of nanos translation initiate during oogenesis and that translational repression is initially independent of Smaug, an embryonic repressor of nanos. Repression during oogenesis and embryogenesis are mediated by distinct stem loops within the nanos 3′ untranslated region; the Smaug-binding stem-loop acts strictly in the embryo, whereas a second stem-loop functions in the oocyte. Thus, independent regulatory modules with temporally distinct activities contribute to spatial regulation of nanos translation. We propose that nanos evolved to exploit two different stage-specific translational regulatory mechanisms.

Multiple mechanisms collaborate to repress nanos translation in the Drosophila ovary and embryo

“…During the latter period of oogenesis, the nurse cells initiate apoptosis and ''dump'' their contents, including nos, into the oocyte (Becalska and Gavis 2009). A small fraction (4%) of nos then becomes localized to the specialized germ plasm at the oocyte posterior, providing a concentrated local source for production of Nos protein (Bergsten and Gavis 1999;Forrest and Gavis 2003;Forrest et al 2004). The remainder of nos that enters the oocyte is translationally silenced (Forrest et al 2004).…”

“…A small fraction (4%) of nos then becomes localized to the specialized germ plasm at the oocyte posterior, providing a concentrated local source for production of Nos protein (Bergsten and Gavis 1999;Forrest and Gavis 2003;Forrest et al 2004). The remainder of nos that enters the oocyte is translationally silenced (Forrest et al 2004). This translational repression of unlocalized nos, coupled with the selective translation of nos localized to the germ plasm, persists in the early embryo, limiting the accumulation of Nos to the posterior region (Gavis and Lehmann 1994).…”

“…The TCE comprises two stemloops, designated II and III, that exhibit developmentally distinct activities through their interactions with repressor proteins (Crucs et al 2000;Forrest et al 2004). Stemloop II mediates repression strictly during embryogenesis, through its interaction with Smaug (Smg), a SAM-domain protein whose own synthesis is repressed during oogenesis (Dahanukar et al 1999;Smibert et al 1999;Forrest et al 2004).…”

“…The TCE comprises two stemloops, designated II and III, that exhibit developmentally distinct activities through their interactions with repressor proteins (Crucs et al 2000;Forrest et al 2004). Stemloop II mediates repression strictly during embryogenesis, through its interaction with Smaug (Smg), a SAM-domain protein whose own synthesis is repressed during oogenesis (Dahanukar et al 1999;Smibert et al 1999;Forrest et al 2004). Smg binds to a motif in stem-loop II designated as the Smg recognition element (SRE), and mutation of either the SRE or Smg itself results in ectopic nos activity in the early embryo (Smibert et al 1996;Dahanukar et al 1999).…”

Emerging Roles for hnRNPs in post-transcriptional regulation: what can we learn from flies?

“…3c). Repression of unlocalized nos is mediated by a bipartite translational control element (TCE) at its 3' untranslated region by the interaction with the Smaug repressor (Smg) (Smibert et al 1999;Forrest et al 2004) (Fig. 3c).…”