The Cytoplasmic Dynein and Kinesin Motors Have Interdependent Roles in Patterning the Drosophila Oocyte

Abstract

Background: Motor proteins of the minus end-directed cytoplasmic dynein and plus end-directed kinesin families provide the principal means for microtubule-based transport in eukaryotic cells. Despite their opposing polarity, these two classes of motors may cooperate in vivo. In Drosophila circumstantial evidence suggests that dynein acts in the localization of determinants and signaling factors during oogenesis. However, the pleiotropic requirement for dynein throughout development has made it difficult to establish its specific role.Results: We analyzed dynein function in the oocyte by disrupting motor activity through temporally restricted expression of the dynactin subunit, dynamitin. Our results indicate that dynein is required for several processes that impact patterning; such processes include localization of bicoid (bcd) and gurken (grk) mRNAs and anchoring of the oocyte nucleus to the cell cortex. Surprisingly, dynein function is sensitive to reduction in kinesin levels, and germ line clones lacking kinesin show defects in dorsal follicle cell fate, grk mRNA localization, and nuclear attachment that are similar to those resulting from the loss of dynein. Significantly, dynein and dynactin localization is perturbed in these animals. Conversely, kinesin localization also depends on dynein activity.Conclusions: We demonstrate that dynein is required for nuclear anchoring and localization of cellular determinants during oogenesis. Strikingly, mutations in the kinesin motor also disrupt these processes and perturb dynein and dynactin localization. These results indicate that the activity of the two motors is interdependent and suggest a model in which kinesin affects patterning indirectly through its role in the localization and recycling of dynein.