Abstract
orb is a founding member of the CPEB family of translational regulators and is required at multiple steps during Drosophila oogenesis. Previous studies showed that orb is required during mid-oogenesis for the translation of the posterior/germline determinant oskar mRNA and the dorsal-ventral determinant gurken mRNA. Here, we report that orb also functions upstream of these axes determinants in the polarization of the microtubule network (MT). Prior to oskar and gurken translational activation, the oocyte MT network is repolarized. The MT organizing center at the oocyte posterior is disassembled, and a new MT network is established at the oocyte anterior. Repolarization depends upon cross-regulatory interactions between anterior (apical) and posterior (basal) Par proteins. We show that repolarization of the oocyte also requires orb and that orb is needed for the proper functioning of the Par proteins. orb interacts genetically with aPKC and cdc42 and in egg chambers compromised for orb activity, Par-1 and aPKC protein and aPKC mRNA are mislocalized. Moreover, like cdc42-, the defects in Par protein localization appear to be connected to abnormalities in the cortical actin cytoskeleton. These abnormalities also disrupt the localization of the spectraplakin Shot and the microtubule minus-end binding protein Patronin. These two proteins play a critical role in the repolarization of the MT network.
Highlights
Specification of the anterior-posterior (AP) and dorsal-ventral (DV) axes of the Drosophila embryo depends upon determinants that are localized within the egg during oogenesis [1,2,3,4]
The specification of polarity axes in the Drosophila egg and embryo depends on the proper organization of the microtubule (MT) and actin cytoskeleton during mid-oogenesis
Consistent with a role for Orb in anchoring aPKC mRNA during midoogenesis, we find that the anterior and lateral cortex associated aPKC mRNA is either partially (Fig 5C) or largely (Fig 5D & 5E) lost when orb activity is depleted by RNAi
Summary
Specification of the anterior-posterior (AP) and dorsal-ventral (DV) axes of the Drosophila embryo depends upon determinants that are localized within the egg during oogenesis [1,2,3,4]. A microtubule organizing center (MTOC) is assembled at the oocyte cortex just posterior to the oocyte nucleus and it directs the elaboration of the MT network by anchoring the minus-ends of MTs. As a consequence of this polarization of the oocyte, mRNAs encoding determinants critical for the early stages (stage 1–7) of egg chamber development accumulate at the posterior cortex. As a consequence of this polarization of the oocyte, mRNAs encoding determinants critical for the early stages (stage 1–7) of egg chamber development accumulate at the posterior cortex One of these is gurken (grk) mRNA. Grk protein translated from this localized message signals to the somatic follicle cells covering the posterior of the egg chamber to specify posterior follicle cell fate (PFC) [7, 8]. Grk protein expressed from the localized message signals dorsal follicle cell fate and this defines the DV axis of the egg chamber and embryo [6, 23]
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