AIR-2: An Aurora/Ipl1-related Protein Kinase Associated with Chromosomes and Midbody Microtubules Is Required for Polar Body Extrusion and Cytokinesis in Caenorhabditis elegans Embryos

Abstract

An emerging family of kinases related to the Drosophila Aurora and budding yeast Ipl1 proteins has been implicated in chromosome segregation and mitotic spindle formation in a number of organisms. Unlike other Aurora/Ipl1-related kinases, the Caenorhabditis elegans orthologue, AIR-2, is associated with meiotic and mitotic chromosomes. AIR-2 is initially localized to the chromosomes of the most mature prophase I–arrested oocyte residing next to the spermatheca. This localization is dependent on the presence of sperm in the spermatheca. After fertilization, AIR-2 remains associated with chromosomes during each meiotic division. However, during both meiotic anaphases, AIR-2 is present between the separating chromosomes. AIR-2 also remains associated with both extruded polar bodies. In the embryo, AIR-2 is found on metaphase chromosomes, moves to midbody microtubules at anaphase, and then persists at the cytokinesis remnant. Disruption of AIR-2 expression by RNA- mediated interference produces entire broods of one-cell embryos that have executed multiple cell cycles in the complete absence of cytokinesis. The embryos accumulate large amounts of DNA and microtubule asters. Polar bodies are not extruded, but remain in the embryo where they continue to replicate. The cytokinesis defect appears to be late in the cell cycle because transient cleavage furrows initiate at the proper location, but regress before the division is complete. Additionally, staining with a marker of midbody microtubules 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 that during each meiotic and mitotic division, AIR-2 may coordinate the congression of metaphase chromosomes with the subsequent events of polar body extrusion and cytokinesis.

Centromere Targeting of the Chromosomal Passenger Complex Requires a Ternary Subcomplex of Borealin, Survivin, and the N-Terminal Domain of INCENP

“…However, consistent with the well documented requirement for Aurora B kinase for chromosome segregation (Schumacher et al, 1998;Adams et al, 2001b;Giet and Glover, 2001;Ditchfield et al, 2003;Hauf et al, 2003), a functional rescue, as judged by the ability of the transfected cells to recruit the spindle checkpoint component BubR1 (Ditchfield et al, 2003;Hauf et al, 2003) or to form a properly aligned metaphase plate, was not observed in INCENP siRNA-treated cells that had been transfected with GFP-INCENP 1-58 (Figure 6, D and E).…”

A cytokinesis furrow is positioned by two consecutive signals

“…3b). These genes have known roles in spindle midzone formation and completion of cytokinesis [17][18][19] . After ASS the aster-positioned furrow ingressed weakly compared with wild-type embryos.…”

Identification of the Substrates and Interaction Proteins of Aurora Kinases from a Protein-Protein Interaction Model

“…In yeast, Ipl1 is normally localized to the spindle pole body (8), and, during mitosis, it is mainly associated with the kinetochore and the mitotic spindles (9). In C. elegans, AIR-1 is localized at the centrosomes (10), while AIR-2 is localized at the kinetochore and midbody (11). In Drosophila, only the centrosome-associated Aurora-A has been thoroughly studied (12).…”