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SOLO: a meiotic protein required for centromere cohesion, coorientation, and SMC1 localization in Drosophila melanogaster.

Yan R, Thomas SE, Tsai JH, Yamada Y, McKee BD - J. Cell Biol. (2010)

Bottom Line: Centromeric foci of the cohesin protein SMC1 are absent in solo mutants at all meiotic stages.SOLO and SMC1 colocalize to meiotic centromeres from early prophase I until anaphase II in wild-type males, but both proteins disappear prematurely at anaphase I in mutants for mei-S332, which encodes the Drosophila homologue of the cohesin protector protein shugoshin.The solo mutant phenotypes and the localization patterns of SOLO and SMC1 indicate that they function together to maintain sister chromatid cohesion in Drosophila meiosis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, Cellular, and Molecular Biology, University of Tennessee, Knoxville, TN 37996, USA.

ABSTRACT
Sister chromatid cohesion is essential to maintain stable connections between homologues and sister chromatids during meiosis and to establish correct centromere orientation patterns on the meiosis I and II spindles. However, the meiotic cohesion apparatus in Drosophila melanogaster remains largely uncharacterized. We describe a novel protein, sisters on the loose (SOLO), which is essential for meiotic cohesion in Drosophila. In solo mutants, sister centromeres separate before prometaphase I, disrupting meiosis I centromere orientation and causing nondisjunction of both homologous and sister chromatids. Centromeric foci of the cohesin protein SMC1 are absent in solo mutants at all meiotic stages. SOLO and SMC1 colocalize to meiotic centromeres from early prophase I until anaphase II in wild-type males, but both proteins disappear prematurely at anaphase I in mutants for mei-S332, which encodes the Drosophila homologue of the cohesin protector protein shugoshin. The solo mutant phenotypes and the localization patterns of SOLO and SMC1 indicate that they function together to maintain sister chromatid cohesion in Drosophila meiosis.

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Colocalization of Venus::SOLO and SMC1 foci on centromeres in WT and mei-S332 spermatocytes. Venus::SOLO and SMC1 foci were detected by anti-GFP and anti-SMC1, respectively, and DNA was stained with DAPI. (A and B) Venus::SOLO and SMC1 foci colocalize until anaphase II in WT (A) but are lost by anaphase I in mei-S332 (B). Arrows point to colocalizing foci. Mutant spermatocytes are from mei-S3324/mei-S3328; {UASp-Venus::SOLO}/{nos-GAL4::VP16} males. All images are sum projections of 3D-deconvolved z series planes. S1 and S2, early prophase I; S6, late prophase I; PMI, prometaphase I; AI, anaphase I; MI, metaphase I; MII, metaphase II. Bars, 1 µm.
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fig7: Colocalization of Venus::SOLO and SMC1 foci on centromeres in WT and mei-S332 spermatocytes. Venus::SOLO and SMC1 foci were detected by anti-GFP and anti-SMC1, respectively, and DNA was stained with DAPI. (A and B) Venus::SOLO and SMC1 foci colocalize until anaphase II in WT (A) but are lost by anaphase I in mei-S332 (B). Arrows point to colocalizing foci. Mutant spermatocytes are from mei-S3324/mei-S3328; {UASp-Venus::SOLO}/{nos-GAL4::VP16} males. All images are sum projections of 3D-deconvolved z series planes. S1 and S2, early prophase I; S6, late prophase I; PMI, prometaphase I; AI, anaphase I; MI, metaphase I; MII, metaphase II. Bars, 1 µm.

Mentions: To determine whether SOLO functions together with a member of the cohesin complex, we compared the localization patterns of SOLO and the cohesin protein SMC1 in spermatocytes from males expressing Venus::SOLO and stained with anti-SMC1 antibody (Fig. 7 A). Anti-SMC1 foci were present at all stages of meiosis I and at metaphase II. In all spermatocytes we examined, anti-SMC1 and Venus::SOLO foci colocalized throughout meiosis until anaphase II, when both proteins became undetectable. These data strongly suggest that SOLO and SMC1 function together to maintain cohesion between sister centromeres in male meiosis. The absence of noncentromeric SMC1 foci during middle and late prophase I was expected from prior observations (Vazquez et al. 2002) that arm cohesion is absent during those stages.


SOLO: a meiotic protein required for centromere cohesion, coorientation, and SMC1 localization in Drosophila melanogaster.

Yan R, Thomas SE, Tsai JH, Yamada Y, McKee BD - J. Cell Biol. (2010)

Colocalization of Venus::SOLO and SMC1 foci on centromeres in WT and mei-S332 spermatocytes. Venus::SOLO and SMC1 foci were detected by anti-GFP and anti-SMC1, respectively, and DNA was stained with DAPI. (A and B) Venus::SOLO and SMC1 foci colocalize until anaphase II in WT (A) but are lost by anaphase I in mei-S332 (B). Arrows point to colocalizing foci. Mutant spermatocytes are from mei-S3324/mei-S3328; {UASp-Venus::SOLO}/{nos-GAL4::VP16} males. All images are sum projections of 3D-deconvolved z series planes. S1 and S2, early prophase I; S6, late prophase I; PMI, prometaphase I; AI, anaphase I; MI, metaphase I; MII, metaphase II. Bars, 1 µm.
© Copyright Policy - openaccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2819681&req=5

fig7: Colocalization of Venus::SOLO and SMC1 foci on centromeres in WT and mei-S332 spermatocytes. Venus::SOLO and SMC1 foci were detected by anti-GFP and anti-SMC1, respectively, and DNA was stained with DAPI. (A and B) Venus::SOLO and SMC1 foci colocalize until anaphase II in WT (A) but are lost by anaphase I in mei-S332 (B). Arrows point to colocalizing foci. Mutant spermatocytes are from mei-S3324/mei-S3328; {UASp-Venus::SOLO}/{nos-GAL4::VP16} males. All images are sum projections of 3D-deconvolved z series planes. S1 and S2, early prophase I; S6, late prophase I; PMI, prometaphase I; AI, anaphase I; MI, metaphase I; MII, metaphase II. Bars, 1 µm.
Mentions: To determine whether SOLO functions together with a member of the cohesin complex, we compared the localization patterns of SOLO and the cohesin protein SMC1 in spermatocytes from males expressing Venus::SOLO and stained with anti-SMC1 antibody (Fig. 7 A). Anti-SMC1 foci were present at all stages of meiosis I and at metaphase II. In all spermatocytes we examined, anti-SMC1 and Venus::SOLO foci colocalized throughout meiosis until anaphase II, when both proteins became undetectable. These data strongly suggest that SOLO and SMC1 function together to maintain cohesion between sister centromeres in male meiosis. The absence of noncentromeric SMC1 foci during middle and late prophase I was expected from prior observations (Vazquez et al. 2002) that arm cohesion is absent during those stages.

Bottom Line: Centromeric foci of the cohesin protein SMC1 are absent in solo mutants at all meiotic stages.SOLO and SMC1 colocalize to meiotic centromeres from early prophase I until anaphase II in wild-type males, but both proteins disappear prematurely at anaphase I in mutants for mei-S332, which encodes the Drosophila homologue of the cohesin protector protein shugoshin.The solo mutant phenotypes and the localization patterns of SOLO and SMC1 indicate that they function together to maintain sister chromatid cohesion in Drosophila meiosis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, Cellular, and Molecular Biology, University of Tennessee, Knoxville, TN 37996, USA.

ABSTRACT
Sister chromatid cohesion is essential to maintain stable connections between homologues and sister chromatids during meiosis and to establish correct centromere orientation patterns on the meiosis I and II spindles. However, the meiotic cohesion apparatus in Drosophila melanogaster remains largely uncharacterized. We describe a novel protein, sisters on the loose (SOLO), which is essential for meiotic cohesion in Drosophila. In solo mutants, sister centromeres separate before prometaphase I, disrupting meiosis I centromere orientation and causing nondisjunction of both homologous and sister chromatids. Centromeric foci of the cohesin protein SMC1 are absent in solo mutants at all meiotic stages. SOLO and SMC1 colocalize to meiotic centromeres from early prophase I until anaphase II in wild-type males, but both proteins disappear prematurely at anaphase I in mutants for mei-S332, which encodes the Drosophila homologue of the cohesin protector protein shugoshin. The solo mutant phenotypes and the localization patterns of SOLO and SMC1 indicate that they function together to maintain sister chromatid cohesion in Drosophila meiosis.

Show MeSH
Related in: MedlinePlus