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The Genetics of Axis Specification in Drosophila
The anterior-posterior polarity of the embryo is established while the oocyte is still in the egg chamber, and it involves interactions between the developing egg cell and the follicular cells that enclose it. The follicular epithelium surrounding the developing oocyte is initially uniform with respect to cell fate, but this uniformity is broken by two signals organized by the oocyte nucleus. Interestingly, both of these signals involve the same gene, gurken. The gurken message appears to be synthesized in the nurse cells, but it is transported into the oocyte. Here it becomes localized between the oocyte nucleus and the cell membrane, and it is translated into Gurken protein (Cáceres and Nilson 2005). At this time the oocyte nucleus is very near what will become the posterior tip of the egg chamber, and the Gurken signal is received by the follicle cells at that position through a receptor protein encoded by the torpedo gene[i] (Figure 1A). This signal results in the “posteriorization” of these follicle cells (Figure 1B). The posterior follicle cells send a signal back into the oocyte. This signaling activates a lipid kinase that recruits the Par-1 protein to the posterior edge of the oocyte cytoplasm (Figure 1A; Doerflinger et al. 2006; Gervais et al. 2008). Par-1 protein organizes microtubules specifically with their minus (cap) and plus (growing) ends at the anterior and posterior ends of the oocyte, respectively (Gonzalez-Reyes et al. 1995; Roth et al. 1995; Januschke et al. 2006).
The orientation of the microtubules is critical, because different microtubule motor proteins will transport their mRNA or protein cargoes in different directions. The motor protein kinesin, for instance, is an ATPase that will use the energy of ATP to transport material to the plus end of the microtubule. Dynein, however, is a “minus-directed” motor protein that transports its cargo in the opposite direction. One of the messages transported by kinesin along the microtubules to the posterior end of the oocyte is oskar mRNA (Zimyanin et al. 2008). The oskar mRNA is not able to be translated until it reaches the posterior cortex, at which time it generates the Oskar protein. Oskar recruits more Par-1 protein, thereby stabilizing the microtubule orientation and allowing more material to be recruited to the posterior pole of the oocyte (Doerflinger et al. 2006; Zimyanin et al. 2007). The posterior pole will thereby have its own distinctive cytoplasm, called pole plasm, which contains the determinants for producing the abdomen and the germ cells.
This cytoskeletal rearrangement in the oocyte is accompanied by an increase in oocyte volume, owing to transfer of cytoplasmic components from the nurse cells. These components include maternal messages such as the bicoid and nanos mRNAs. These mRNAs are carried by motor proteins along the microtubules to the anterior and posterior ends of the oocyte, respectively (Figure 1D-F). The protein products encoded by bicoid and nanos are critical for establishing the anterior-posterior polarity of the embryo.
[i] Gurken protein is a member of the EGF (epidermal growth factor) family, and torpedo encodes a homologue of the vertebrate EGF receptor (Price et al. 1989; Neuman-Silberberg and Schüpbach 1993).
Literature Cited
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