Lighting up mRNA localization inDrosophilaoogenesis

Abstract

The asymmetric localization of four maternal mRNAs - gurken, bicoid,oskar and nanos - in the Drosophila oocyte is essential for the development of the embryonic body axes. Fluorescent imaging methods are now being used to visualize these mRNAs in living tissue, allowing dynamic analysis of their behaviors throughout the process of localization. This review summarizes recent findings from such studies that provide new insight into the elaborate cellular mechanisms that are used to transport mRNAs to different regions of the oocyte and to maintain their localized distributions during oogenesis.

Early asymmetries in maternal transcript distribution associated with a cortical microtubule network and a polar body in the beetle Tribolium castaneum

“…The strong and discrete signal obtained for T.c.pangolin is reminiscent of that from mRNA transport ''particles'' and/ or localized mRNA foci in Drosophila oocytes (Weil et al, 2008;Becalska and Gavis, 2009) and may represent similar particles involved in the transport and/or anchoring of T.c.pangolin transcripts in Tribolium. Indeed, the structure of the CMN we describe here is also interesting in light of recent work on the mechanism of oskar mRNA localization in Drosophila (Zimyanin et al, 2008).…”

“…mRNA localization is emerging as a powerful means by which polarity is established at the cellular level, for example, in the establishment of axial polarity in oocytes (King et al, 2005;Becalska and Gavis, 2009), in the control of fibroblast migration (Condeelis and Singer, 2005), or in axon guidance in neurons (Martin et al, 2000). Since one mRNA can be translated many times, mRNA localization is an efficient mechanism to localize proteins at high concentrations, with regulation at the translational level facilitating rapid changes in protein levels in response to fluctuations in local conditions.…”

“…All animals develop from a single cell, and thus it is not surprising that mRNA localization is also found to play a role in the initial establishment of embryonic axes in a wide variety of species (Singer, 2008;Becalska and Gavis, 2009). Data emerging from studies on a number of insects suggest that the localization of maternal mRNAs plays a prominent role in axis specification within this group of arthropods.…”

“…Two well-studied examples of longgerm holometabolous insects are the fruitfly Drosophila melanogaster and the parasitic wasp Nasonia vitripennis. In Drosophila, the anterior-posterior (AP) and dorsal-ventral (DV) axes are established via the asymmetric localization of four maternal mRNAs during oogenesis (Becalska and Gavis, 2009): gurken, bicoid, oskar, and nanos. gurken mRNAs encode an EGF signaling pathway ligand of the tgfa family and exhibit a spatiotemporally dynamic behaviour during oogenesis, first localizing to the posterior and then later anteriodorsally, playing a central role in the establishment of both the AP and DV axes (MacDougall et al, 2003), while the anterior localization of bicoid mRNAs (Clark et al, 2007;Weil et al, 2008) and the posterior localization of oskar and nanos mRNAs (Wang et al, 1994;Zimyanin et al, 2008) are together essential for correct AP axis specification.…”

“…gurken mRNAs encode an EGF signaling pathway ligand of the tgfa family and exhibit a spatiotemporally dynamic behaviour during oogenesis, first localizing to the posterior and then later anteriodorsally, playing a central role in the establishment of both the AP and DV axes (MacDougall et al, 2003), while the anterior localization of bicoid mRNAs (Clark et al, 2007;Weil et al, 2008) and the posterior localization of oskar and nanos mRNAs (Wang et al, 1994;Zimyanin et al, 2008) are together essential for correct AP axis specification. The efficient localization of gurken, bicoid, and oskar mRNAs during oogenesis is dependent on active transport along microtubules mediated by the plus-end-directed motor protein kinesin (for oskar) or the minus-end-directed motor protein dynein (for gurken and bicoid), in addition to transcript, microtubule, and/or motor protein-specific cofactors (Becalska and Gavis, 2009). In Nasonia, broad embryonic patterning gradients are also established via the maternal localization of transcripts, although the maternal genes involved in AP axis specification largely differ from those in Drosophila (for a discussion on the evolutionary significance of this, see Peel, 2008): giant maternal mRNAs are localized to the anterior pole, caudal and nanos maternal mRNAs are localized to the posterior pole, while orthodenticle-1 maternal mRNAs are localized to both poles (Lynch et al, 2006;Olesnicky et al, 2006;Brent et al, 2007;Olesnicky and Desplan, 2007).…”