The centrosome-nucleus complex and microtubule organization in theDrosophilaoocyte

Abstract

Molecular motors transport the axis-determining mRNAs oskar, bicoid and gurken along microtubules (MTs) in the Drosophila oocyte. However, it remains unclear how the underlying MT network is organized and how this transport takes place. We have identified a centriole-containing centrosome close to the oocyte nucleus. Remarkably, the centrosomal components, ␥-tubulin and Drosophila pericentrin-like protein also strongly accumulate at the periphery of this nucleus. MT polymerization after cold-induced disassembly in wild type and in gurken mutants suggests that in the oocyte the centrosome-nucleus complex is an active center of MT polymerization. We further report that the MT network comprises two perpendicular MT subsets that undergo dynamic rearrangements during oogenesis. This MT reorganization parallels the successive steps in localization of gurken and oskar mRNAs. We propose that in addition to a highly polarized microtubule scaffold specified by the cortex oocyte, the repositioning of the nucleus and its tightly associated centrosome could control MT reorganization and, hence, oocyte polarization.

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

“…The precise organization of microtubules in Drosophila oocytes has long remained unclear and controversial. One reason for this might be a rapid turnover or rearrangement of microtubules in Drosophila oocytes (Januschke et al, 2006). Using live imaging of fluorescently labeled transcripts, Zimyanin et al (2008) demonstrated that oskar mRNA particles localize to the posterior via a posteriorly biased random walk, using a microtubule network that is only weakly polarized along the anteriorposterior axis.…”

Microtubule polarity and axis formation in theDrosophila oocyte

“…Steinhauer, unpublished data). ␥-tubulin isoforms also have been found associated with the oocyte nucleus, and one very recent study hypothesized that the oocyte nucleus is the primary locus of MT nucleating activity in the oocyte (Januschke et al, 2006). In that study, complete depolymerization of oocyte MTs followed by short recovery periods revealed that at stage 9, oocyte MTs regrow from a site at the dorsal anterior corner, near the oocyte nucleus.…”

“…As a result, it was hypothesized that the posterior MTOC established at stage 2 persists aberrantly after stage 7 in grk mutants (Roth et al, 1995). Januschke et al (2006) propose an alternate model, whereby the posteriorly positioned oocyte nucleus is responsible for the high concentration of posterior MTs in grk mutant oocytes. However, this alternate model cannot account for the aberrant MTs at the posterior of the oocyte in other mutant backgrounds, e.g., in PKA mutants, in which nuclear migration to the dorsal anterior corner occurs normally (see below).…”

In vivo analysis of MT‐based vesicle transport by confocal reflection microscopy

“…The MTs form loose, long parallel bundles perpendicular to the anterior-posterior axis of the oocyte, close to the egg cortex [Januschke et al, 2006]. Most of the cytoplasm components travel along the bundles with a seemingly smooth movement with no mayor changes in direction and velocity.…”

“…The MTs become depolymerized during incubation on ice and form again once the egg primordia are transferred onto to 258C [Januschke et al, 2006]. Imaging of one early stage 12 oocyte per preparation was done in every minute, as described above.…”