Limits...
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.

Show MeSH

Related in: MedlinePlus

AIR-2 is localized to meiotic chromosomes. Gonads were dissected from wild-type adult hermaphrodites, fixed, and then  stained with DAPI (A, E, I, M, and Q), AIR-2 antisera (B, F, J, N, R, and T), and α-tubulin antisera (C, G, K, and O). Merged images  are shown in D, H, L, and P. (A–D) AIR-2 is diffuse throughout the distal and proximal gonad, but is specifically localized to chromosomes in the oocyte most proximal to the spermatheca (white box). The spermatheca is to the left of the white box in A–D, but is out of  the focal plane. (E–H) High magnification of the most proximal oocyte (boxed region in A–D). AIR-2 is specifically localized to meiotic  chromosomes in the proximal oocyte. (I–L) Meiosis resumes after the oocyte is ovulated into the spermatheca and is fertilized. AIR-2 is  associated with the chromosomes undergoing meiotic divisions (arrows). The sperm chromatin is visible at the posterior in I. Left, anterior. (M–P) AIR-2 is localized between the chromosomes during meiotic anaphase (arrows). Left, anterior. (Q and R) Polar bodies are  extruded after each meiotic division at the anterior of the embryo. AIR-2 staining remains on the polar bodies throughout their presence during embryogenesis. AIR-2 staining is not associated with maternal or paternal pronuclear chromatin (the two nuclei within the  embryo, Q). Left, anterior. (S and T) AIR-2 stains the mature sperm found in hermaphrodites but appears to be distinct from the chromatin. AIR-2 was also found in mature sperm from males (data not shown). Bars: (A–D) 50 μm; (E–H, I–L, M–P, Q, and R) 10 μm.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2132979&req=5

Figure 3: AIR-2 is localized to meiotic chromosomes. Gonads were dissected from wild-type adult hermaphrodites, fixed, and then stained with DAPI (A, E, I, M, and Q), AIR-2 antisera (B, F, J, N, R, and T), and α-tubulin antisera (C, G, K, and O). Merged images are shown in D, H, L, and P. (A–D) AIR-2 is diffuse throughout the distal and proximal gonad, but is specifically localized to chromosomes in the oocyte most proximal to the spermatheca (white box). The spermatheca is to the left of the white box in A–D, but is out of the focal plane. (E–H) High magnification of the most proximal oocyte (boxed region in A–D). AIR-2 is specifically localized to meiotic chromosomes in the proximal oocyte. (I–L) Meiosis resumes after the oocyte is ovulated into the spermatheca and is fertilized. AIR-2 is associated with the chromosomes undergoing meiotic divisions (arrows). The sperm chromatin is visible at the posterior in I. Left, anterior. (M–P) AIR-2 is localized between the chromosomes during meiotic anaphase (arrows). Left, anterior. (Q and R) Polar bodies are extruded after each meiotic division at the anterior of the embryo. AIR-2 staining remains on the polar bodies throughout their presence during embryogenesis. AIR-2 staining is not associated with maternal or paternal pronuclear chromatin (the two nuclei within the embryo, Q). Left, anterior. (S and T) AIR-2 stains the mature sperm found in hermaphrodites but appears to be distinct from the chromatin. AIR-2 was also found in mature sperm from males (data not shown). Bars: (A–D) 50 μm; (E–H, I–L, M–P, Q, and R) 10 μm.

Mentions: Immunocytochemistry using affinity-purified AIR-2 antisera on fixed gonads dissected from gravid adult wild-type hermaphrodites revealed that the AIR-2 protein was specifically localized to meiotic chromosomes (Fig. 3). The C. elegans gonad can be divided into three separate regions: (a) the distal syncytial gonad, which is populated by mitotic germ cells, (b) the syncytial meiotic region, which is characterized by the presence of hundreds of germ nuclei arrested in pachytene of meiosis I, and (c) the proximal gonad (next to the spermatheca and uterus) where oocytes begin to cellularize around nuclei containing condensed meiotic chromosomes in diakinesis of prophase I (Schedl, 1997).


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 localized to meiotic chromosomes. Gonads were dissected from wild-type adult hermaphrodites, fixed, and then  stained with DAPI (A, E, I, M, and Q), AIR-2 antisera (B, F, J, N, R, and T), and α-tubulin antisera (C, G, K, and O). Merged images  are shown in D, H, L, and P. (A–D) AIR-2 is diffuse throughout the distal and proximal gonad, but is specifically localized to chromosomes in the oocyte most proximal to the spermatheca (white box). The spermatheca is to the left of the white box in A–D, but is out of  the focal plane. (E–H) High magnification of the most proximal oocyte (boxed region in A–D). AIR-2 is specifically localized to meiotic  chromosomes in the proximal oocyte. (I–L) Meiosis resumes after the oocyte is ovulated into the spermatheca and is fertilized. AIR-2 is  associated with the chromosomes undergoing meiotic divisions (arrows). The sperm chromatin is visible at the posterior in I. Left, anterior. (M–P) AIR-2 is localized between the chromosomes during meiotic anaphase (arrows). Left, anterior. (Q and R) Polar bodies are  extruded after each meiotic division at the anterior of the embryo. AIR-2 staining remains on the polar bodies throughout their presence during embryogenesis. AIR-2 staining is not associated with maternal or paternal pronuclear chromatin (the two nuclei within the  embryo, Q). Left, anterior. (S and T) AIR-2 stains the mature sperm found in hermaphrodites but appears to be distinct from the chromatin. AIR-2 was also found in mature sperm from males (data not shown). Bars: (A–D) 50 μm; (E–H, I–L, M–P, Q, and R) 10 μm.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: AIR-2 is localized to meiotic chromosomes. Gonads were dissected from wild-type adult hermaphrodites, fixed, and then stained with DAPI (A, E, I, M, and Q), AIR-2 antisera (B, F, J, N, R, and T), and α-tubulin antisera (C, G, K, and O). Merged images are shown in D, H, L, and P. (A–D) AIR-2 is diffuse throughout the distal and proximal gonad, but is specifically localized to chromosomes in the oocyte most proximal to the spermatheca (white box). The spermatheca is to the left of the white box in A–D, but is out of the focal plane. (E–H) High magnification of the most proximal oocyte (boxed region in A–D). AIR-2 is specifically localized to meiotic chromosomes in the proximal oocyte. (I–L) Meiosis resumes after the oocyte is ovulated into the spermatheca and is fertilized. AIR-2 is associated with the chromosomes undergoing meiotic divisions (arrows). The sperm chromatin is visible at the posterior in I. Left, anterior. (M–P) AIR-2 is localized between the chromosomes during meiotic anaphase (arrows). Left, anterior. (Q and R) Polar bodies are extruded after each meiotic division at the anterior of the embryo. AIR-2 staining remains on the polar bodies throughout their presence during embryogenesis. AIR-2 staining is not associated with maternal or paternal pronuclear chromatin (the two nuclei within the embryo, Q). Left, anterior. (S and T) AIR-2 stains the mature sperm found in hermaphrodites but appears to be distinct from the chromatin. AIR-2 was also found in mature sperm from males (data not shown). Bars: (A–D) 50 μm; (E–H, I–L, M–P, Q, and R) 10 μm.
Mentions: Immunocytochemistry using affinity-purified AIR-2 antisera on fixed gonads dissected from gravid adult wild-type hermaphrodites revealed that the AIR-2 protein was specifically localized to meiotic chromosomes (Fig. 3). The C. elegans gonad can be divided into three separate regions: (a) the distal syncytial gonad, which is populated by mitotic germ cells, (b) the syncytial meiotic region, which is characterized by the presence of hundreds of germ nuclei arrested in pachytene of meiosis I, and (c) the proximal gonad (next to the spermatheca and uterus) where oocytes begin to cellularize around nuclei containing condensed meiotic chromosomes in diakinesis of prophase I (Schedl, 1997).

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