Polo kinase Cdc5 is a central regulator of meiosis I

被引:46
作者
Attner, Michelle A. [1 ]
Miller, Matthew P. [1 ]
Ee, Ly-sha [1 ]
Elkin, Sheryl K. [1 ]
Amon, Angelika [1 ,2 ]
机构
[1] MIT, Dept Biol, David H Koch Inst Integrat Canc Res, Cambridge, MA 02139 USA
[2] MIT, Howard Hughes Med Inst, Cambridge, MA 02139 USA
基金
美国国家卫生研究院;
关键词
SINGLE-DIVISION MEIOSIS; BUDDING YEAST MEIOSIS; CHROMOSOME SEGREGATION; SACCHAROMYCES-CEREVISIAE; HOMOLOGOUS CHROMOSOMES; REC8; PHOSPHORYLATION; CENTROMERIC COHESION; MIXED SEGREGATION; ANAPHASE; SPO13;
D O I
10.1073/pnas.1311845110
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
During meiosis, two consecutive rounds of chromosome segregation yield four haploid gametes from one diploid cell. The Polo kinase Cdc5 is required for meiotic progression, but how Cdc5 coordinates multiple cell-cycle events during meiosis I is not understood. Here we show that CDC5-dependent phosphorylation of Rec8, a subunit of the cohesin complex that links sister chromatids, is required for efficient cohesin removal from chromosome arms, which is a prerequisite for meiosis I chromosome segregation. CDC5 also establishes conditions for centromeric cohesin removal during meiosis II by promoting the degradation of Spo13, a protein that protects centromeric cohesin during meiosis I. Despite CDC5's central role in meiosis I, the protein kinase is dispensable during meiosis II and does not even phosphorylate its meiosis I targets during the second meiotic division. We conclude that Cdc5 has evolved into a master regulator of the unique meiosis I chromosome segregation pattern.
引用
收藏
页码:14278 / 14283
页数:6
相关论文
共 33 条
[11]   Regulation of the Bub2/Bfal GAP complex by Cdc5 and cell cycle checkpoints [J].
Hu, FH ;
Wang, YC ;
Liu, D ;
Li, YM ;
Qin, J ;
Elledge, SJ .
CELL, 2001, 107 (05) :655-665
[12]  
HUGERAT Y, 1993, GENETICS, V135, P297
[13]   Rec8 Phosphorylation by Casein Kinase 1 and Cdc7-Dbf4 Kinase Regulates Cohesin Cleavage by Separase during Meiosis [J].
Katis, Vittorio L. ;
Lipp, Jesse J. ;
Imre, Richard ;
Bogdanova, Aliona ;
Okaz, Elwy ;
Habermann, Bianca ;
Mechtler, Karl ;
Nasmyth, Kim ;
Zachariae, Wolfgang .
DEVELOPMENTAL CELL, 2010, 18 (03) :397-409
[14]   Spo13 facilitates monopolin recruitment to kinetochores and regulates maintenance of centromeric cohesion during yeast meiosis [J].
Katis, VL ;
Matos, J ;
Mori, S ;
Shirahige, K ;
Zachariae, W ;
Nasmyth, K .
CURRENT BIOLOGY, 2004, 14 (24) :2183-2196
[15]   Spo13 maintains centromeric cohesion and kinetochore coorientation during meiosis I [J].
Lee, BH ;
Kiburz, BM ;
Amon, A .
CURRENT BIOLOGY, 2004, 14 (24) :2168-2182
[16]   Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation [J].
Lee, BH ;
Amon, A .
SCIENCE, 2003, 300 (5618) :482-486
[17]   Meiosis: Cell-cycle controls shuffle and deal [J].
Marston, AL ;
Amon, A .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2004, 5 (12) :983-997
[18]   The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation [J].
Marston, AL ;
Lee, BH ;
Amon, A .
DEVELOPMENTAL CELL, 2003, 4 (05) :711-726
[19]   Dbf4-Dependent Cdc7 Kinase Links DNA Replication to the Segregation of Homologous Chromosomes in Meiosis I [J].
Matos, Joao ;
Lipp, Jesse J. ;
Bogdanova, Aliona ;
Guillot, Sylvine ;
Okaz, Elwy ;
Junqueira, Magno ;
Shevchenko, Andrej ;
Zachariae, Wolfgang .
CELL, 2008, 135 (04) :662-678
[20]   Meiosis I chromosome segregation is established through regulation of microtubule-kinetochore interactions [J].
Miller, Matthew P. ;
Uenal, Elcin ;
Brar, Gloria A. ;
Amon, Angelika .
ELIFE, 2012, 1