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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 member of a highly conserved  family of protein kinases. An alignment of the  predicted protein product sequences for C. elegans AIR-2 and AIR-1, mammalian AIM-1 and  IAK-1, Drosophila Aurora, and budding yeast  Ipl1 is shown. Black shading, identical residues;  gray shading, similar residues; underline, predicted kinase domain. The AIR-2 kinase domain  has the following amino acid identities and similarities with the kinase domains of (a) AIM-1:  63% identical, 76% similar; (b) IAK-1: 62%  identical, 75% similar; (c) Aurora: 55% identical, 71% similar; (d) AIR-1: 51% identical, 69%  similar; and (e) Ipl1: 50% identical, 70% similar.  Nucleotide and predicted protein sequences for  the air-2 cDNA have been submitted to GenBank/EMBL/DDBJ under accession number  AF071207.
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Figure 1: AIR-2 is member of a highly conserved family of protein kinases. An alignment of the predicted protein product sequences for C. elegans AIR-2 and AIR-1, mammalian AIM-1 and IAK-1, Drosophila Aurora, and budding yeast Ipl1 is shown. Black shading, identical residues; gray shading, similar residues; underline, predicted kinase domain. The AIR-2 kinase domain has the following amino acid identities and similarities with the kinase domains of (a) AIM-1: 63% identical, 76% similar; (b) IAK-1: 62% identical, 75% similar; (c) Aurora: 55% identical, 71% similar; (d) AIR-1: 51% identical, 69% similar; and (e) Ipl1: 50% identical, 70% similar. Nucleotide and predicted protein sequences for the air-2 cDNA have been submitted to GenBank/EMBL/DDBJ under accession number AF071207.

Mentions: We have identified two new members of the Aurora/Ipl1 protein kinase family, AIR-1 and AIR-2, in the C. elegans genome database. Further analysis of AIR-1 has been presented elsewhere (Schumacher et al., 1998). The air-2 genomic sequence was found on cosmid B0207 from chromosome I (B0207; GenBank/EMBL/DDBJ accession number U97196). B0207 maps to the right of dpy-5 and to the left of bli-4. An oligonucleotide primer corresponding to the SL1 trans-spliced leader RNA (found on the majority of C. elegans mRNAs) (Blumenthal, 1995), and a primer specific for the region surrounding the predicted translation stop codon of the air-2 sequence were used to RT-PCR amplify an air-2 cDNA from adult C. elegans hermaphrodite total RNA. Sequencing of the air-2 cDNA revealed that it lacked the first exon predicted by the C. elegans Genome Consortium, but otherwise reflected the predicted exon structure. An alignment of the predicted protein sequences for C. elegans AIR-2 and AIR-1, mammalian AIM-1 and IAK-1, Drosophila Aurora, and yeast Ipl1, showed that all six coding regions share a high degree of homology throughout the predicted kinase domain and only diverge significantly at their amino termini (Fig. 1).


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 member of a highly conserved  family of protein kinases. An alignment of the  predicted protein product sequences for C. elegans AIR-2 and AIR-1, mammalian AIM-1 and  IAK-1, Drosophila Aurora, and budding yeast  Ipl1 is shown. Black shading, identical residues;  gray shading, similar residues; underline, predicted kinase domain. The AIR-2 kinase domain  has the following amino acid identities and similarities with the kinase domains of (a) AIM-1:  63% identical, 76% similar; (b) IAK-1: 62%  identical, 75% similar; (c) Aurora: 55% identical, 71% similar; (d) AIR-1: 51% identical, 69%  similar; and (e) Ipl1: 50% identical, 70% similar.  Nucleotide and predicted protein sequences for  the air-2 cDNA have been submitted to GenBank/EMBL/DDBJ under accession number  AF071207.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2132979&req=5

Figure 1: AIR-2 is member of a highly conserved family of protein kinases. An alignment of the predicted protein product sequences for C. elegans AIR-2 and AIR-1, mammalian AIM-1 and IAK-1, Drosophila Aurora, and budding yeast Ipl1 is shown. Black shading, identical residues; gray shading, similar residues; underline, predicted kinase domain. The AIR-2 kinase domain has the following amino acid identities and similarities with the kinase domains of (a) AIM-1: 63% identical, 76% similar; (b) IAK-1: 62% identical, 75% similar; (c) Aurora: 55% identical, 71% similar; (d) AIR-1: 51% identical, 69% similar; and (e) Ipl1: 50% identical, 70% similar. Nucleotide and predicted protein sequences for the air-2 cDNA have been submitted to GenBank/EMBL/DDBJ under accession number AF071207.
Mentions: We have identified two new members of the Aurora/Ipl1 protein kinase family, AIR-1 and AIR-2, in the C. elegans genome database. Further analysis of AIR-1 has been presented elsewhere (Schumacher et al., 1998). The air-2 genomic sequence was found on cosmid B0207 from chromosome I (B0207; GenBank/EMBL/DDBJ accession number U97196). B0207 maps to the right of dpy-5 and to the left of bli-4. An oligonucleotide primer corresponding to the SL1 trans-spliced leader RNA (found on the majority of C. elegans mRNAs) (Blumenthal, 1995), and a primer specific for the region surrounding the predicted translation stop codon of the air-2 sequence were used to RT-PCR amplify an air-2 cDNA from adult C. elegans hermaphrodite total RNA. Sequencing of the air-2 cDNA revealed that it lacked the first exon predicted by the C. elegans Genome Consortium, but otherwise reflected the predicted exon structure. An alignment of the predicted protein sequences for C. elegans AIR-2 and AIR-1, mammalian AIM-1 and IAK-1, Drosophila Aurora, and yeast Ipl1, showed that all six coding regions share a high degree of homology throughout the predicted kinase domain and only diverge significantly at their amino termini (Fig. 1).

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