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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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Cohesion of sister centromeres is lost by late prophase I in solo mutants. (A, B, and D) Testes from WT (A), solo/Df(2L)A267 (B), and rescued solo (solo/Df(2L)A267; {UASp-Venus::SOLO}/{nos-GAL4::VP16}) (D) males stained with anti-CID antibody to identify centromeres and with DAPI to visualize DNA. Sum or maximum projections of 3D-deconvolved z series stacks were performed to obtain CID signals. No more than eight CID spots are present in WT meiosis I at any stage, whereas solo spermatocytes show more than eight CID spots at late prophase I, prometaphase I, and metaphase I (11, 13, and 15 spots, respectively, in the nuclei shown). Arrows indicate a bivalent with four fully separated sister centromeres. S3, mid–prophase I; S5, late prophase I; PMI, prometaphase I; MI, metaphase I; MII, metaphase II. Bars, 5 µm. (C) Quantification of CID spots in (soloZ2-0198/Df(2L)A267) at different stages. The percent of spermatocytes with more than eight spots is shown. The number of nuclei scored is in parentheses.
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fig4: Cohesion of sister centromeres is lost by late prophase I in solo mutants. (A, B, and D) Testes from WT (A), solo/Df(2L)A267 (B), and rescued solo (solo/Df(2L)A267; {UASp-Venus::SOLO}/{nos-GAL4::VP16}) (D) males stained with anti-CID antibody to identify centromeres and with DAPI to visualize DNA. Sum or maximum projections of 3D-deconvolved z series stacks were performed to obtain CID signals. No more than eight CID spots are present in WT meiosis I at any stage, whereas solo spermatocytes show more than eight CID spots at late prophase I, prometaphase I, and metaphase I (11, 13, and 15 spots, respectively, in the nuclei shown). Arrows indicate a bivalent with four fully separated sister centromeres. S3, mid–prophase I; S5, late prophase I; PMI, prometaphase I; MI, metaphase I; MII, metaphase II. Bars, 5 µm. (C) Quantification of CID spots in (soloZ2-0198/Df(2L)A267) at different stages. The percent of spermatocytes with more than eight spots is shown. The number of nuclei scored is in parentheses.

Mentions: To examine the cohesive status of sister centromeres during meiosis I more globally, we made use of an antibody against centromere identifier (CID), a centromere-specific histone H3–like protein (Ahmad and Henikoff, 2001; Blower and Karpen, 2001) that enables visualization of all centromeres simultaneously (Fig. 4). In WT spermatocytes, the number of anti-CID foci per nucleus never exceeded the number of homologous chromosomes (eight in meiosis I and four in meiosis II). During late prophase I when the four bivalents occupy well-separated territories, two CID spots could often be seen in each chromosome territory.


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)

Cohesion of sister centromeres is lost by late prophase I in solo mutants. (A, B, and D) Testes from WT (A), solo/Df(2L)A267 (B), and rescued solo (solo/Df(2L)A267; {UASp-Venus::SOLO}/{nos-GAL4::VP16}) (D) males stained with anti-CID antibody to identify centromeres and with DAPI to visualize DNA. Sum or maximum projections of 3D-deconvolved z series stacks were performed to obtain CID signals. No more than eight CID spots are present in WT meiosis I at any stage, whereas solo spermatocytes show more than eight CID spots at late prophase I, prometaphase I, and metaphase I (11, 13, and 15 spots, respectively, in the nuclei shown). Arrows indicate a bivalent with four fully separated sister centromeres. S3, mid–prophase I; S5, late prophase I; PMI, prometaphase I; MI, metaphase I; MII, metaphase II. Bars, 5 µm. (C) Quantification of CID spots in (soloZ2-0198/Df(2L)A267) at different stages. The percent of spermatocytes with more than eight spots is shown. The number of nuclei scored is in parentheses.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2819681&req=5

fig4: Cohesion of sister centromeres is lost by late prophase I in solo mutants. (A, B, and D) Testes from WT (A), solo/Df(2L)A267 (B), and rescued solo (solo/Df(2L)A267; {UASp-Venus::SOLO}/{nos-GAL4::VP16}) (D) males stained with anti-CID antibody to identify centromeres and with DAPI to visualize DNA. Sum or maximum projections of 3D-deconvolved z series stacks were performed to obtain CID signals. No more than eight CID spots are present in WT meiosis I at any stage, whereas solo spermatocytes show more than eight CID spots at late prophase I, prometaphase I, and metaphase I (11, 13, and 15 spots, respectively, in the nuclei shown). Arrows indicate a bivalent with four fully separated sister centromeres. S3, mid–prophase I; S5, late prophase I; PMI, prometaphase I; MI, metaphase I; MII, metaphase II. Bars, 5 µm. (C) Quantification of CID spots in (soloZ2-0198/Df(2L)A267) at different stages. The percent of spermatocytes with more than eight spots is shown. The number of nuclei scored is in parentheses.
Mentions: To examine the cohesive status of sister centromeres during meiosis I more globally, we made use of an antibody against centromere identifier (CID), a centromere-specific histone H3–like protein (Ahmad and Henikoff, 2001; Blower and Karpen, 2001) that enables visualization of all centromeres simultaneously (Fig. 4). In WT spermatocytes, the number of anti-CID foci per nucleus never exceeded the number of homologous chromosomes (eight in meiosis I and four in meiosis II). During late prophase I when the four bivalents occupy well-separated territories, two CID spots could often be seen in each chromosome territory.

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