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

doi:10.1083/jcb.143.6.1635

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© The Rockefeller University Press, 0021-9525/1998//1635 $5.00
The Journal of Cell Biology, Volume 143, Number 6, , 1998 1635-1646

Article

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

Jill M. Schumacher^*^,, Andy Golden, and Peter J. Donovan^*

^* Cell Biology of Development and Differentiation Group and Developmental Signal Transduction Group, ABL-Basic Research Program, NCI-Frederick Cancer Research and Development Center, Frederick, Maryland 21702

An emerging family of kinases related to the Drosophila Auroraand budding yeast Ipl1 proteins has been implicated in chromosomesegregation and mitotic spindle formation in a number of organisms.Unlike other Aurora/Ipl1-related kinases, the Caenorhabditiselegans orthologue, AIR-2, is associated with meiotic and mitoticchromosomes. AIR-2 is initially localized to the chromosomesof the most mature prophase I–arrested oocyte residingnext to the spermatheca. This localization is dependent on thepresence of sperm in the spermatheca. After fertilization,AIR-2 remains associated with chromosomes during each meioticdivision. However, during both meiotic anaphases, AIR-2 ispresent between the separating chromosomes. AIR-2 also remainsassociated with both extruded polar bodies. In the embryo, AIR-2is found on metaphase chromosomes, moves to midbody microtubulesat anaphase, and then persists at the cytokinesis remnant.Disruption of AIR-2 expression by RNA- mediated interferenceproduces entire broods of one-cell embryos that have executedmultiple cell cycles in the complete absence of cytokinesis.The embryos accumulate large amounts of DNA and microtubuleasters. Polar bodies are not extruded, but remain in the embryowhere they continue to replicate. The cytokinesis defect appearsto be late in the cell cycle because transient cleavage furrowsinitiate at the proper location, but regress before the divisionis complete. Additionally, staining with a marker of midbodymicrotubules revealed that at least some of the components of the midbody are not well localized in the absence of AIR-2activity. Our results suggest that during each meiotic andmitotic division, AIR-2 may coordinate the congression of metaphasechromosomes with the subsequent events of polar body extrusionand cytokinesis.

Key Words: cytokinesis • Aurora • chromosomes • meiosis • polar bodies • RNAi

Abbreviations used in this paper: AIR, Aurora/Ipl1 related protein; DAPI, 4',6-diamidino-3-phenylindole dihydrochloride; gf, gain-of-function; KLH, keyhole limpet hemacyanin; RNAi, RNA-mediated interference.

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