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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.

Schumacher JM, Golden A, Donovan PJ - J. Cell Biol. (1998)

Bottom Line: Unlike other Aurora/Ipl1-related kinases, the Caenorhabditis elegans orthologue, AIR-2, is associated with meiotic and mitotic 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.

View Article: PubMed Central - PubMed

Affiliation: Cell Biology of Development and Differentiation Group, ABL-Basic Research Program, NCI-Frederick Cancer Research and Development Center, Frederick, Maryland 21702, USA.

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.

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AIR-2 is retained at  the cytokinesis remnant. (A– L) Embryos were dissected  from wild-type adult hermaphrodites, fixed, and then stained  with DAPI (A, E, and I), AIR-2  (B, F, and J), and actin antibodies (C, G, and K). Merged  images are shown in (D, H,  and L). (A–D) AIR-2 is concentrated between separating  chromatin at anaphase. The  AB cell in anterior (left) is in  telophase, the P1 cell in posterior (right) is in anaphase. (E– H) AIR-2 staining persists on  the cell membrane once cytokinesis is complete (arrowhead).  The dot of staining that is not  associated with the membrane  is a polar body that is out of  the focal plane. (I–L) AIR-2  appears to behave similarly  throughout embryogenesis in  all cell lineages. Bar, 10 μm.
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Figure 6: AIR-2 is retained at the cytokinesis remnant. (A– L) Embryos were dissected from wild-type adult hermaphrodites, fixed, and then stained with DAPI (A, E, and I), AIR-2 (B, F, and J), and actin antibodies (C, G, and K). Merged images are shown in (D, H, and L). (A–D) AIR-2 is concentrated between separating chromatin at anaphase. The AB cell in anterior (left) is in telophase, the P1 cell in posterior (right) is in anaphase. (E– H) AIR-2 staining persists on the cell membrane once cytokinesis is complete (arrowhead). The dot of staining that is not associated with the membrane is a polar body that is out of the focal plane. (I–L) AIR-2 appears to behave similarly throughout embryogenesis in all cell lineages. Bar, 10 μm.

Mentions: To confirm the various subcellular locations of AIR-2 during the cell cycle, fixed embryos of varying ages were coimmunostained with AIR-2– and actin-specific antibodies. Again, AIR-2 was present between the chromosomes in anaphase and telophase (Fig. 6, A–D), and was found as a small dot of staining on the cell membrane following cytokinesis (Fig. 6, E–H). All of the cell cycle–specific AIR-2 staining patterns described were found throughout the embryo and were not cell lineage-specific (Fig. 6, I–L, and data not shown). Given that the AIR-2 protein was present during gametogenesis and throughout embryogenesis, AIR-2 is likely to be both a maternally supplied and a zygotically expressed gene product.


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.

Schumacher JM, Golden A, Donovan PJ - J. Cell Biol. (1998)

AIR-2 is retained at  the cytokinesis remnant. (A– L) Embryos were dissected  from wild-type adult hermaphrodites, fixed, and then stained  with DAPI (A, E, and I), AIR-2  (B, F, and J), and actin antibodies (C, G, and K). Merged  images are shown in (D, H,  and L). (A–D) AIR-2 is concentrated between separating  chromatin at anaphase. The  AB cell in anterior (left) is in  telophase, the P1 cell in posterior (right) is in anaphase. (E– H) AIR-2 staining persists on  the cell membrane once cytokinesis is complete (arrowhead).  The dot of staining that is not  associated with the membrane  is a polar body that is out of  the focal plane. (I–L) AIR-2  appears to behave similarly  throughout embryogenesis in  all cell lineages. Bar, 10 μm.
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Related In: Results  -  Collection

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Figure 6: AIR-2 is retained at the cytokinesis remnant. (A– L) Embryos were dissected from wild-type adult hermaphrodites, fixed, and then stained with DAPI (A, E, and I), AIR-2 (B, F, and J), and actin antibodies (C, G, and K). Merged images are shown in (D, H, and L). (A–D) AIR-2 is concentrated between separating chromatin at anaphase. The AB cell in anterior (left) is in telophase, the P1 cell in posterior (right) is in anaphase. (E– H) AIR-2 staining persists on the cell membrane once cytokinesis is complete (arrowhead). The dot of staining that is not associated with the membrane is a polar body that is out of the focal plane. (I–L) AIR-2 appears to behave similarly throughout embryogenesis in all cell lineages. Bar, 10 μm.
Mentions: To confirm the various subcellular locations of AIR-2 during the cell cycle, fixed embryos of varying ages were coimmunostained with AIR-2– and actin-specific antibodies. Again, AIR-2 was present between the chromosomes in anaphase and telophase (Fig. 6, A–D), and was found as a small dot of staining on the cell membrane following cytokinesis (Fig. 6, E–H). All of the cell cycle–specific AIR-2 staining patterns described were found throughout the embryo and were not cell lineage-specific (Fig. 6, I–L, and data not shown). Given that the AIR-2 protein was present during gametogenesis and throughout embryogenesis, AIR-2 is likely to be both a maternally supplied and a zygotically expressed gene product.

Bottom Line: Unlike other Aurora/Ipl1-related kinases, the Caenorhabditis elegans orthologue, AIR-2, is associated with meiotic and mitotic 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.

View Article: PubMed Central - PubMed

Affiliation: Cell Biology of Development and Differentiation Group, ABL-Basic Research Program, NCI-Frederick Cancer Research and Development Center, Frederick, Maryland 21702, USA.

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.

Show MeSH
Related in: MedlinePlus