AIR-2: An Aurora/Ip11-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos

An emerging family of kinases related to the Drosophila Aurora and budding yeast Ipl1 proteins has been implicated in chromosome segregation and mitot ic spindle formation in a number of organisms. Unlike other Aurora/Ipl1-rel ated kinases, the Caenorhabditis elegans orthologue, AIR-2, is associated w ith meiotic and mitotic chromosomes. AIR-2 is initially localized to the ch romosomes of the most mature prophase I-arrested oocyte residing next to th e spermatheca. This localization is dependent on the presence of sperm in t he spermatheca. After fertilization, AIR-2 remains associated with chromoso mes during each meiotic division. However, during both meiotic anaphases, A IR-2 is present between the separating chromosomes. AIR-2 also remains asso ciated with both extruded polar bodies. In the embryo, AIR-2 is found on me taphase chromosomes, moves to midbody microtubules at anaphase, and then pe rsists at the cytokinesis remnant. Disruption of AIR-2 expression by RNA-me diated interference produces entire broods of one-cell embryos that have ex ecuted multiple cell cycles in the complete absence of cytokinesis. The emb ryos accumulate large amounts of DNA and microtubule asters. Polar bodies a re not extruded, but remain in the embryo where they continue to replicate. The cytokinesis defect appears to be late in the cell cycle because transi ent cleavage furrows initiate at the proper location, but regress before th e division is complete. Additionally, staining with a marker of midbody mic rotubules revealed that at least some of the components of the midbody are not well localized in the absence of AIR-2 activity. Our results suggest th at during each meiotic and mitotic division, AIR-2 may coordinate the congr ession of metaphase chromosomes with the subsequent events of polar body ex trusion and cytokinesis.