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Spindle checkpoint activation at meiosis I advances anaphase II onset via meiosis-specific APC/C regulation.

Yamamoto A, Kitamura K, Hihara D, Hirose Y, Katsuyama S, Hiraoka Y - J. Cell Biol. (2008)

Bottom Line: Furthermore, anaphase onset was advanced and the SAC effect was reduced at meiosis II.The advancement of anaphase onset depended on a meiosis-specific, Cdc20-related factor, Fzr1/Mfr1, which contributed to anaphase cyclin decline and anaphase onset and was inefficiently inhibited by the SAC.Our findings show that impacts of SAC activation are not confined to a single division at meiosis due to meiosis-specific APC/C regulation, which has probably been evolved for execution of two meiotic divisions.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, Shizuoka University, Suruga-ku, Shizuoka 422-8529, Japan. sayamam@ipc.shizuoka.ac.jp

ABSTRACT
During mitosis, the spindle assembly checkpoint (SAC) inhibits the Cdc20-activated anaphase-promoting complex/cyclosome (APC/C(Cdc20)), which promotes protein degradation, and delays anaphase onset to ensure accurate chromosome segregation. However, the SAC function in meiotic anaphase regulation is poorly understood. Here, we examined the SAC function in fission yeast meiosis. As in mitosis, a SAC factor, Mad2, delayed anaphase onset via Slp1 (fission yeast Cdc20) when chromosomes attach to the spindle improperly. However, when the SAC delayed anaphase I, the interval between meiosis I and II shortened. Furthermore, anaphase onset was advanced and the SAC effect was reduced at meiosis II. The advancement of anaphase onset depended on a meiosis-specific, Cdc20-related factor, Fzr1/Mfr1, which contributed to anaphase cyclin decline and anaphase onset and was inefficiently inhibited by the SAC. Our findings show that impacts of SAC activation are not confined to a single division at meiosis due to meiosis-specific APC/C regulation, which has probably been evolved for execution of two meiotic divisions.

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Dynamics of the chromosome, the spindle, and Cdc13 at MI in rec12 mutant. (A) Behavior of homologous centromeres and the SPB at MI. Arrowheads indicate the homologous centromeres (cen2). Bottom panels highlight independent oscillations of the homologous centromeres (white and red arrowheads) at phase II. The graph shows changes in the SPB-cen (D1 and D2) and SPB-SPB (D3) distances. (B) Behavior of the MI spindle in rec12. The arrow in the top graph shows the sudden regression of the spindle. Arrowheads indicate the thin spindle midzone. Dotted lines in graphs show boundaries of the spindle phases. PI, phase I; PII, phase II; PIII, phase III. (C) Duration of spindle phases. (D) Dynamics of Cdc13-GFP at MI. (E) Timing of arm locus separation at MI. Bars show time of separation of the ade6, ade8, and sod2 loci after spindle formation. At least seven cells were examined for each locus. Wt, wild type. Error bars indicate standard deviation. Bars: (A, top, B, and D) 5 μm; (A, bottom) 2 μm.
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fig2: Dynamics of the chromosome, the spindle, and Cdc13 at MI in rec12 mutant. (A) Behavior of homologous centromeres and the SPB at MI. Arrowheads indicate the homologous centromeres (cen2). Bottom panels highlight independent oscillations of the homologous centromeres (white and red arrowheads) at phase II. The graph shows changes in the SPB-cen (D1 and D2) and SPB-SPB (D3) distances. (B) Behavior of the MI spindle in rec12. The arrow in the top graph shows the sudden regression of the spindle. Arrowheads indicate the thin spindle midzone. Dotted lines in graphs show boundaries of the spindle phases. PI, phase I; PII, phase II; PIII, phase III. (C) Duration of spindle phases. (D) Dynamics of Cdc13-GFP at MI. (E) Timing of arm locus separation at MI. Bars show time of separation of the ade6, ade8, and sod2 loci after spindle formation. At least seven cells were examined for each locus. Wt, wild type. Error bars indicate standard deviation. Bars: (A, top, B, and D) 5 μm; (A, bottom) 2 μm.

Mentions: Analysis of the chromosome dynamics confirmed improper spindle attachment of chromosomes at MI in rec12. Homologous centromeres oscillated between the two poles independently of each other, with kinetic parameters similar to those in the wild type (Fig. 2 A, top, PII; Fig. 2 A, bottom; Fig. 2 A, top right, D1 and D2; and Table S2) and with frequent arrival at the poles before anaphase I (Fig. 2 A, top, 12 min; and Fig. 2 A, bottom, 16, 19, and 27 min); they frequently segregated to the same pole (3 out of 7 cases; Fig. 2 A, top, 59 min). In addition, sister centromeres occasionally underwent equational segregation (2 of 14 cases). Thus, both bipolar attachment of homologues and monopolar attachment of sister chromatids were perturbed in rec12.


Spindle checkpoint activation at meiosis I advances anaphase II onset via meiosis-specific APC/C regulation.

Yamamoto A, Kitamura K, Hihara D, Hirose Y, Katsuyama S, Hiraoka Y - J. Cell Biol. (2008)

Dynamics of the chromosome, the spindle, and Cdc13 at MI in rec12 mutant. (A) Behavior of homologous centromeres and the SPB at MI. Arrowheads indicate the homologous centromeres (cen2). Bottom panels highlight independent oscillations of the homologous centromeres (white and red arrowheads) at phase II. The graph shows changes in the SPB-cen (D1 and D2) and SPB-SPB (D3) distances. (B) Behavior of the MI spindle in rec12. The arrow in the top graph shows the sudden regression of the spindle. Arrowheads indicate the thin spindle midzone. Dotted lines in graphs show boundaries of the spindle phases. PI, phase I; PII, phase II; PIII, phase III. (C) Duration of spindle phases. (D) Dynamics of Cdc13-GFP at MI. (E) Timing of arm locus separation at MI. Bars show time of separation of the ade6, ade8, and sod2 loci after spindle formation. At least seven cells were examined for each locus. Wt, wild type. Error bars indicate standard deviation. Bars: (A, top, B, and D) 5 μm; (A, bottom) 2 μm.
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Related In: Results  -  Collection

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fig2: Dynamics of the chromosome, the spindle, and Cdc13 at MI in rec12 mutant. (A) Behavior of homologous centromeres and the SPB at MI. Arrowheads indicate the homologous centromeres (cen2). Bottom panels highlight independent oscillations of the homologous centromeres (white and red arrowheads) at phase II. The graph shows changes in the SPB-cen (D1 and D2) and SPB-SPB (D3) distances. (B) Behavior of the MI spindle in rec12. The arrow in the top graph shows the sudden regression of the spindle. Arrowheads indicate the thin spindle midzone. Dotted lines in graphs show boundaries of the spindle phases. PI, phase I; PII, phase II; PIII, phase III. (C) Duration of spindle phases. (D) Dynamics of Cdc13-GFP at MI. (E) Timing of arm locus separation at MI. Bars show time of separation of the ade6, ade8, and sod2 loci after spindle formation. At least seven cells were examined for each locus. Wt, wild type. Error bars indicate standard deviation. Bars: (A, top, B, and D) 5 μm; (A, bottom) 2 μm.
Mentions: Analysis of the chromosome dynamics confirmed improper spindle attachment of chromosomes at MI in rec12. Homologous centromeres oscillated between the two poles independently of each other, with kinetic parameters similar to those in the wild type (Fig. 2 A, top, PII; Fig. 2 A, bottom; Fig. 2 A, top right, D1 and D2; and Table S2) and with frequent arrival at the poles before anaphase I (Fig. 2 A, top, 12 min; and Fig. 2 A, bottom, 16, 19, and 27 min); they frequently segregated to the same pole (3 out of 7 cases; Fig. 2 A, top, 59 min). In addition, sister centromeres occasionally underwent equational segregation (2 of 14 cases). Thus, both bipolar attachment of homologues and monopolar attachment of sister chromatids were perturbed in rec12.

Bottom Line: Furthermore, anaphase onset was advanced and the SAC effect was reduced at meiosis II.The advancement of anaphase onset depended on a meiosis-specific, Cdc20-related factor, Fzr1/Mfr1, which contributed to anaphase cyclin decline and anaphase onset and was inefficiently inhibited by the SAC.Our findings show that impacts of SAC activation are not confined to a single division at meiosis due to meiosis-specific APC/C regulation, which has probably been evolved for execution of two meiotic divisions.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, Shizuoka University, Suruga-ku, Shizuoka 422-8529, Japan. sayamam@ipc.shizuoka.ac.jp

ABSTRACT
During mitosis, the spindle assembly checkpoint (SAC) inhibits the Cdc20-activated anaphase-promoting complex/cyclosome (APC/C(Cdc20)), which promotes protein degradation, and delays anaphase onset to ensure accurate chromosome segregation. However, the SAC function in meiotic anaphase regulation is poorly understood. Here, we examined the SAC function in fission yeast meiosis. As in mitosis, a SAC factor, Mad2, delayed anaphase onset via Slp1 (fission yeast Cdc20) when chromosomes attach to the spindle improperly. However, when the SAC delayed anaphase I, the interval between meiosis I and II shortened. Furthermore, anaphase onset was advanced and the SAC effect was reduced at meiosis II. The advancement of anaphase onset depended on a meiosis-specific, Cdc20-related factor, Fzr1/Mfr1, which contributed to anaphase cyclin decline and anaphase onset and was inefficiently inhibited by the SAC. Our findings show that impacts of SAC activation are not confined to a single division at meiosis due to meiosis-specific APC/C regulation, which has probably been evolved for execution of two meiotic divisions.

Show MeSH
Related in: MedlinePlus