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First published online January 14, 2005
doi: 10.1242/10.1242/jcs.01637

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RNA localization mechanisms in oocytes

Department of Molecular Genetics, The University of Texas, M. D. Anderson Cancer Center, Houston, TX 77030, USA

View larger version (32K): [in a new window]   Fig. 1. Pathways of RNA localization in Xenopus oogenesis. (A) The early (METRO) localization pathway operates in early oogenesis (stages I and II) and uses the mitochondrial cloud (Balbiani body) to localize RNAs such as Xcat2 mRNA (red) and noncoding Xlsirts RNA (blue) to the vegetal pole of the oocyte. (1) In stage I oocytes, RNAs synthesized in the nucleus (yellow) enter (either via nuage or by the diffusion/entrapment mechanism) the mitochondrial cloud (mitochondria shown in green), which faces the vegetal pole of the oocyte. Xcat2 mRNA becomes localized to the germinal granules (red spheres) and Xlsirts RNA is localized between the germinal granules at the vegetal apex (METRO region) of the mitochondrial cloud. (2) In stage II oocytes, the mitochondrial cloud moves to the vegetal cortex and starts to disperse. (3) In stage III-VI oocytes, the mitochondrial cloud disperses, and germinal granules and localized RNAs form a disc at the apex of the vegetal cortex. (B) The late (Vg1) pathway localizes mRNAs such as Vg1 or VegT, using MTs, molecular motors and possibly the ER. (4) In stage I oocytes, these RNAs (purple) are uniformly distributed within the oocyte cytoplasm and are excluded from the mitochondrial cloud. (5) In late stage II oocytes, RNAs concentrate, in a wedge, around the moving mitochondrial cloud and a subdomain of ER, and translocate on MTs towards the vegetal pole. (6) Later in oogenesis (stages III-VI), late-pathway RNAs localize and anchor at the cortex of the vegetal half of the oocyte (for details, see Kloc and Etkin, 1995).

View larger version (60K): [in a new window]   Fig. 2. Balbiani body in the oocytes of insects and Xenopus. (A) Fragment of the ovariole from the ovary of the cricket Acheta domesticus seen with a Nomarski contrast microscope. This is a panoistic type of ovary. In this type of ovary (unlike in the meroistic type found in Drosophila), there are no nurse cells, and the oocyte nucleus (the germinal vesicle, GV) is large and transcriptionally active. In the previtellogenic oocytes (on the left), there is one Balbiani body (arrow) located at the anterior pole of the oocyte. In older oocytes, there are two Balbiani bodies, one at the anterior and another at the posterior pole (marked by a star) (for details, see Bradley et al., 2001). (B) Balbiani bodies (mitochondrial clouds) in stage I and stage II Xenopus oocytes. Whole mount in situ hybridization with antisense Xcat2 probe shows that Xcat2 mRNA is localized in the mitochondrial cloud (arrow), which always faces the vegetal pole (star) of the oocyte. In stage I oocytes, the mitochondrial cloud is located close to the GV and, in stage II oocytes, the mitochondrial cloud translocates to the vegetal pole. (C) Mitochondrial cloud from stage I Xenopus oocyte. Three-dimensional reconstruction from 21 serial electron microscopic sections of an oocyte hybridized to the Xcat2 RNA probe, artificially colored. Germinal granules (arrows indicate the individual granules), labeled with Xcat2 mRNA (red), are located between the mitochondria and concentrated in the METRO region at the vegetal apex (star) of the cloud (for details, see Kloc et al., 2002). Bar, 60 µm in A, 120 µm in B, and 6 µm in C.

View larger version (19K): [in a new window]   Fig. 3. Model of the action of Halo-like proteins in bidirectional transport on MTs. (A) In the absence of Halo proteins, plus-end and minus-end motors alternate their binding to coordination machinery (possibly containing dynactin) and move RNA cargo towards either plus-ends or minus-ends of MTs. (B) Halo proteins change the steric properties of the coordination machinery, which weakens its binding to the minus-end motor and increases its binding to the plus-end motor, and results in the movement of the cargo towards the MT plus-end [adapted from Gross (Gross, 2003) and Gross et al. (Gross et al., 2003)].

View larger version (25K): [in a new window]   Fig. 4. Transport and anchoring of oskar mRNA in Drosophila oogenesis. (1) In early oogenesis (stage 2-6), the MTs extend from the oocyte posterior to the nurse cells. Then, oskar mRNA is transported from the nurse cells, on the MTs, via ring canals, to the posterior cortex of the oocyte. (2) In mid oogenesis (stage 8), there is a re-polarization of the oocyte MTs, the MTOC at the oocyte posterior disassembles, and new MTs are nucleated from most of the oocyte cortex. The plus-end-directed motor kinesin transports oskar mRNA away from the cortex and towards the oocyte interior. (3) Subsequent destabilization of MTs at the oocyte posterior (late stage 8 and early stage 9) uncovers the posterior actin anchor, leading to the entrapment and concentration of oskar mRNA at the posterior pole [adapted from Cha et al. (Cha et al., 2004)].

View larger version (24K): [in a new window]   Fig. 5. Model illustrating the dependence of the fate of localized endogenous and exogenous RNAs in Xenopus oogenesis on their nuclear/cytoplasmic history. Endogenous (A) and exogenous (B) early- and late-pathway RNAs. (1) In stage I oocytes, the early-pathway RNAs, such as Xcat2 mRNA, bind nuclear proteins (possibly Sm proteins) that facilitate transport (via nuclear pores) to the mitochondrial cloud (yellow) and germinal granules (red spheres). The late-pathway RNAs, such as Vg1 mRNA, bind to Vg1RPB/Vera and hnRNP, which form a core complex facilitating export from the nucleus, and diffuse uniformly within the oocyte cytoplasm. (2) Later in oogenesis (starting from late stage II or early stage III), Staufen and Prrp proteins are added to the core complex assembled on late-pathway RNAs. These bind to a molecular motor, such as kinesin I and/or II, that transports RNAs on the MT tracks that form a wedge around the remnants of the mitochondrial cloud. (3) Early- and late-pathway RNAs injected into the nuclei of stage I/early stage II oocytes that bind the appropriate nuclear factors and mimic the localization pattern of their endogenous counterparts. There is no information on the fate of early- or late-pathway RNAs injected into the cytoplasm of stage I oocytes. (4) Early-pathway RNAs injected into the nucleus or cytoplasm of stage III, or older, oocytes behave like late-pathway RNAs migrating on the MTs towards the vegetal cortex. This indicates that the early-pathway binding factors present in the nuclei of stage I/early stage II oocytes are either absent or unavailable in older oocytes. However, the early-pathway RNAs can bind some of the cytoplasmic factors of the late-pathway machinery, and they either mimic the movement of late-pathway RNAs or piggyback on late-pathway RNAs. Late-pathway RNAs injected into the nuclei or cytoplasm of older oocytes bind the appropriate factors and after export into the cytoplasm behave like their endogenous counterparts - either assembling their own transport complexes or piggybacking on endogenous RNAs.

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