Sister chromatid segregation in meiosis II : Deprotection through phosphorylation

Cell Cycle

Volumn 12, Issue 9, 2013, Pages 1352-1359

  Wassmann, Katja ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

Author keywords

Cohesin deprotection; Cohesin protection; Cyclin A; I2PP2A Set; Meiosis; Oocytes; PP2A; Rec8; Separase; Shugoshin

Indexed keywords

CASEIN KINASE I; COHESIN; MEMBRANE PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; REC8 PROTEIN; UNCLASSIFIED DRUG;

CATALYSIS; CELL ADHESION; CELL CYCLE PROGRESSION; CELL DIVISION; CELL FUNCTION; CELL STRUCTURE; CENTROMERE; CHROMOSOME SEGREGATION; DEPROTECTION REACTION; HOMOLOGOUS RECOMBINATION; HUMAN; MAMMAL CELL; MEIOSIS; METAPHASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SISTER CHROMATID;

EID: 84877126331     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24600     Document Type: Review

References (100)

1. Lichten M, de Massy B. The impressionistic landscape of meiotic recombination. Cell 2011; 147:267-70; PMID:22000007; http://dx.doi.org/10.1016/ j.cell.2011.09.038
2. Roig I, Keeney S. Probing meiotic recombination decisions. Dev Cell 2008; 15:331-2; PMID:18804427; http://dx.doi.org/10.1016/j.devcel.2008.08.009
3. Petronczki M, Siomos MF, Nasmyth K. Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 2003; 112:423-40; PMID:12600308; http://dx.doi.org/10.1016/S0092-8674(03)00083-7
4. Zickler D, Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet 1999; 33:603-754; PMID:10690419; http://dx.doi.org/10. 1146/annurev.genet.33.1.603
5. Jessberger R. Age-related aneuploidy through cohesion exhaustion. EMBO Rep 2012; 13:539-46; PMID:22565322; http://dx.doi.org/10.1038/embor.2012.54
6. Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 2012; 13:493-504; PMID:22705668; http://dx.doi.org/10.1038/nrg3245
7. Hassold T, Hunt P. Maternal age and chromosomally abnormal pregnancies: what we know and what we wish we knew. Curr Opin Pediatr 2009; 21:703-8; PMID:19881348; http://dx.doi.org/10.1097/MOP.0b013e328332c6ab
8. Page SL, Hawley RS. Chromosome choreography: the meiotic ballet. Science 2003; 301:785-9; PMID:12907787; http://dx.doi.org/10.1126/science.1086605
9. Losada A. Cohesin regulation: fashionable ways to wear a ring. Chromosoma 2007; 116:321-9; PMID:17333234; http://dx.doi.org/10.1007/s00412-007-0104-x
10. Mehta GD, Rizvi SM, Ghosh SK. Cohesin: a guardian of genome integrity. Biochim Biophys Acta 2012; 1823:1324-42; PMID:22677545; http://dx.doi.org/10. 1016/j.bbamcr.2012.05.027
11. Hauf S, Watanabe Y. Kinetochore orientation in mitosis and meiosis. Cell 2004; 119:317-27; PMID:15507205; http://dx.doi.org/10.1016/j.cell.2004.10.014
12. Brar GA, Amon A. Emerging roles for centromeres in meiosis I chromosome segregation. Nat Rev Genet 2008; 9:899-910; PMID:18981989; http://dx.doi.org/10. 1038/nrg2454
13. Marston AL, Amon A. Meiosis: cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 2004; 5:983-97; PMID:15573136; http://dx.doi.org/10.1038/ nrm1526
14. Shintomi K, Hirano T. Sister chromatid resolution: a cohesin releasing network and beyond. Chromosoma 2010; 119:459-67; PMID:20352243; http://dx.doi.org/10.1007/s00412-010-0271-z
15. Hauf S, Roitinger E, Koch B, Dittrich CM, Mechtler K, Peters JM. Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol 2005; 3:e69; PMID:15737063; http://dx.doi.org/10.1371/journal.pbio.0030069
16. Sumara I, Vorlaufer E, Stukenberg PT, Kelm O, Redemann N, Nigg EA, et al. The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase. Mol Cell 2002; 9:515-25; PMID:11931760; http://dx.doi.org/10. 1016/S1097-2765(02)00473-2
17. Shintomi K, Hirano T. Releasing cohesin from chromosome arms in early mitosis: opposing actions of Wapl-Pds5 and Sgo1. Genes Dev 2009; 23:2224-36; PMID:19696148; http://dx.doi.org/10.1101/gad.1844309.
18. Giménez-Abián JF, Sumara I, Hirota T, Hauf S, Gerlich D, de la Torre C, et al. Regulation of sister chromatid cohesion between chromosome arms. Curr Biol 2004; 14:1187-93; PMID:15242616; http://dx.doi.org/10.1016/j. cub.2004.06.052
19. Gandhi R, Gillespie PJ, Hirano T. Human Wapl is a cohesin-binding protein that promotes sisterchromatid resolution in mitotic prophase. Curr Biol 2006; 16:2406-17; PMID:17112726; http://dx.doi.org/10.1016/j.cub.2006.10.061
20. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, et al. Wapl controls the dynamic association of cohesin with chromatin. Cell 2006; 127:955-67; PMID:17113138; http://dx.doi.org/10.1016/j.cell.2006.09.040
21. Nakajima M, Kumada K, Hatakeyama K, Noda T, Peters JM, Hirota T. The complete removal of cohesin from chromosome arms depends on separase. J Cell Sci 2007; 120:4188-96; PMID:18003702; http://dx.doi.org/10.1242/jcs.011528
22. Waizenegger IC, Hauf S, Meinke A, Peters JM. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 2000; 103:399-410; PMID:11081627; http://dx.doi.org/10.1016/ S0092-8674(00)00132-X
23. Hauf S, Waizenegger IC, Peters JM. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 2001; 293:1320-3; PMID:11509732; http://dx.doi.org/10.1126/science.1061376.
24. Wirth KG, Wutz G, Kudo NR, Desdouets C, Zetterberg A, Taghybeeglu S, et al. Separase: a universal trigger for sister chromatid disjunction but not chromosome cycle progression. J Cell Biol 2006; 172:847-60; PMID:16533945; http://dx.doi.org/10.1083/jcb.200506119
25. Kumada K, Yao R, Kawaguchi T, Karasawa M, Hoshikawa Y, Ichikawa K, et al. The selective continued linkage of centromeres from mitosis to interphase in the absence of mammalian separase. J Cell Biol 2006; 172:835-46; PMID:16533944; http://dx.doi.org/10.1083/jcb.200511126
26. Lara-Gonzalez P, Westhorpe FG, Taylor SS. The spindle assembly checkpoint. Curr Biol 2012; 22:R966-80; PMID:23174302; http://dx.doi.org/10. 1016/j.cub.2012.10.006
27. Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 2007; 8:379-93; PMID:17426725; http://dx.doi.org/10. 1038/nrm2163
28. Acquaviva C, Pines J. The anaphase-promoting complex/cyclosome: APC/C. J Cell Sci 2006; 119:2401-4; PMID:16763193; http://dx.doi.org/10.1242/jcs.02937
29. Gorr IH, Boos D, Stemmann O. Mutual inhibition of separase and Cdk1 by two-step complex formation. Mol Cell 2005; 19:135-41; PMID:15989971; http://dx.doi.org/10.1016/j.molcel.2005.05.022
30. Holland AJ, Taylor SS. Cyclin-B1-mediated inhibition of excess separase is required for timely chromosome disjunction. J Cell Sci 2006; 119:3325-36; PMID:16868023; http://dx.doi.org/10.1242/jcs.03083
31. Zou H, McGarry TJ, Bernal T, Kirschner MW. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science 1999; 285:418-22; PMID:10411507; http://dx.doi.org/10. 1126/science.285.5426.418
32. Hagting A, Den Elzen N, Vodermaier HC, Waizenegger IC, Peters JM, Pines J. Human securin proteolysis is controlled by the spindle checkpoint and reveals when the APC/C switches from activation by Cdc20 to Cdh1. J Cell Biol 2002; 157:1125-37; PMID:12070128; http://dx.doi.org/10.1083/jcb.200111001
33. Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, Xu H, et al. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 2006; 126:135-46; PMID:16839882; http://dx.doi.org/10.1016/j.cell.2006.05.033
34. Wassmann K, Niault T, Maro B, Metaphase I. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 2003; 13:1596-608; PMID:13678590; http://dx.doi.org/10.1016/j.cub.2003.08.052
35. Herbert M, Levasseur M, Homer H, Yallop K, Murdoch A, McDougall A. Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat Cell Biol 2003; 5:1023-5; PMID:14593421; http://dx.doi.org/10. 1038/ncb1062
36. Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M. Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 2005; 130:829-43; PMID:16322543; http://dx.doi.org/10.1530/rep.1.00856
37. Homer HA, McDougall A, Levasseur M, Yallop K, Murdoch AP, Herbert M. Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev 2005; 19:202-7; PMID:15655110; http://dx.doi.org/10.1101/gad.328105
38. McGuinness BE, Anger M, Kouznetsova A, Gil-Bernabé AM, Helmhart W, Kudo NR, et al. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol 2009; 19:369-80; PMID:19249208; http://dx.doi.org/10.1016/j.cub.2009.01.064
39. Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, et al. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 1999; 19:3515-28; PMID:10207075
40. Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ. Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 2005; 8:949-61; PMID:15935783; http://dx.doi.org/10.1016/j.devcel.2005.03.018
41. Katis VL, Lipp JJ, Imre R, Bogdanova A, Okaz E, Habermann B, et al. Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 2010; 18:397-409; PMID:20230747; http://dx.doi.org/10.1016/j.devcel.2010.01.014
42. Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, Riedel CG, et al. Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 2010; 9:2657-62; PMID:20581463; http://dx.doi.org/10.4161/cc.9.13.12146
43. Ishiguro T, Tanaka K, Sakuno T, Watanabe Y. Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 2010; 12:500-6; PMID:20383139; http://dx.doi.org/10.1038/ncb2052
44. Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, et al. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 2006; 441:46-52; PMID:16541025; http://dx.doi.org/10.1038/nature04663
45. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 2006; 441:53-61; PMID:16541024; http://dx.doi.org/10.1038/nature04664
46. Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 2004; 427:510-7; PMID:14730319; http://dx.doi.org/10.1038/nature02312
47. Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K. Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 2004; 14:287-301; PMID:14972679
48. Katis VL, Galova M, Rabitsch KP, Gregan J, Nasmyth K. Maintenance of cohesin at centromeres after meiosis I in budding yeast requires a kinetochore-associated protein related to MEI-S332. Curr Biol 2004; 14:560-72; PMID:15062096; http://dx.doi.org/10.1016/j.cub.2004.03.001
49. Marston AL, Tham WH, Shah H, Amon A. A genome-wide screen identifies genes required for centromeric cohesion. Science 2004; 303:1367-70; PMID:14752166; http://dx.doi.org/10.1126/science.1094220
50. Alexandru G, Uhlmann F, Mechtler K, Poupart MA, Nasmyth K. Phosphorylation of the cohesin subunit Scc1 by Polo/Cdc5 kinase regulates sister chromatid separation in yeast. Cell 2001; 105:459-72; PMID:11371343; http://dx.doi.org/10.1016/S0092-8674(01)00362-2
51. Hornig NC, Uhlmann F. Preferential cleavage of chromatin-bound cohesin after targeted phosphorylation by Polo-like kinase. EMBO J 2004; 23:3144-53; PMID:15241476; http://dx.doi.org/10.1038/sj.emboj.7600303
52. Yao Y, Dai W. Shugoshins function as a guardian for chromosomal stability in nuclear division. Cell Cycle 2012; 11:2631-42; PMID:22732496; http://dx.doi.org/10.4161/cc.20633
53. Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, et al. Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 2008; 10:42-52; PMID:18084284; http://dx.doi.org/ 10.1038/ncb1667
54. Kerrebrock AW, Moore DP, Wu JS, Orr-Weaver TL. Mei-S332, a Drosophila protein required for sisterchromatid cohesion, can localize to meiotic centromere regions. Cell 1995; 83:247-56; PMID:7585942; http://dx.doi.org/10. 1016/0092-8674(95)90166-3
55. Gómez R, Valdeolmillos A, Parra MT, Viera A, Carreiro C, Roncal F, et al. Mammalian SGO2 appears at the inner centromere domain and redistributes depending on tension across centromeres during meiosis II and mitosis. EMBO Rep 2007; 8:173-80; PMID:17205076; http://dx.doi.org/10.1038/sj.embor.7400877
56. Gregan J, Rumpf C, Li Z, Cipak L. What makes centromeric cohesion resistant to separase cleavage during meiosis I but not during meiosis II? Cell Cycle 2008; 7:151-3; PMID:18256525; http://dx.doi.org/10.4161/cc.7.2.5325
57. Chambon JP, Touati SA, Berneau S, Cladière D, Hebras C, Groeme R, et al. The PP2A Inhibitor I2PP2A Is Essential for Sister Chromatid Segregation in Oocyte Meiosis II. Curr Biol 2013; 23:485-90; PMID:23434280; http://dx.doi.org/10.1016/j.cub.2013.02.004
58. Lee J, Iwai T, Yokota T, Yamashita M. Temporally and spatially selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis. J Cell Sci 2003; 116:2781-90; PMID:12759374; http://dx.doi.org/10.1242/jcs.00495
59. Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C. Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol 2003; 160:657-70; PMID:12615909; http://dx.doi.org/10.1083/jcb.200212080
60. Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, Adams DJ, et al. Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 2010; 24:2505-16; PMID:20971813; http://dx.doi.org/10.1101/gad.605910
61. Llano E, Gómez R, Gutiérrez-Caballero C, Herrán Y, Sánchez-Martín M, Vázquez-Quiñones L, et al. Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 2008; 22:2400-13; PMID:18765791; http://dx.doi.org/10.1101/gad.475308
62. Mailhes JB, Hilliard C, Fuseler JW, London SN. Okadaic acid, an inhibitor of protein phosphatase 1 and 2A, induces premature separation of sister chromatids during meiosis I and aneuploidy in mouse oocytes in vitro. Chromosome Res 2003; 11:619-31; PMID:14516070; http://dx.doi.org/10.1023/A:1024909119593
63. Chang HY, Jennings PC, Stewart J, Verrills NM, Jones KT. Essential role of protein phosphatase 2A in metaphase II arrest and activation of mouse eggs shown by okadaic acid, dominant negative protein phosphatase 2A, and FTY720. J Biol Chem 2011; 286:14705-12; PMID:21383018; http://dx.doi.org/10.1074/jbc.M110. 193227
64. Domingo-Sananes MR, Kapuy O, Hunt T, Novak B. Switches and latches: a biochemical tug-of-war between the kinases and phosphatases that control mitosis. Philos Trans R Soc Lond B Biol Sci 2011; 366:3584-94; PMID:22084385; http://dx.doi.org/10.1098/rstb.2011.0087
65. Barr FA, Elliott PR, Gruneberg U. Protein phosphatases and the regulation of mitosis. J Cell Sci 2011; 124:2323-34; PMID:21709074; http://dx.doi.org/10. 1242/jcs.087106
66. Vaur S, Cubizolles F, Plane G, Genier S, Rabitsch PK, Gregan J, et al. Control of Shugoshin function during fission-yeast meiosis. Curr Biol 2005; 15:2263-70; PMID:16360688; http://dx.doi.org/10.1016/j.cub.2005.11.034
67. Kouznetsova A, Lister L, Nordenskjöld M, Herbert M, Höög C. Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat Genet 2007; 39:966-8; PMID:17618286; http://dx.doi.org/10.1038/ng2065
68. Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 2010; 20:1522-8; PMID:20817534; http://dx.doi.org/10.1016/j. cub.2010.06.069
69. LeMaire-Adkins R, Hunt PA. Nonrandom segregation of the mouse univalent X chromosome: evidence of spindle-mediated meiotic drive. Genetics 2000; 156:775-83; PMID:11014823
70. Petronczki M, Matos J, Mori S, Gregan J, Bogdanova A, Schwickart M, et al. Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 2006; 126:1049-64; PMID:16990132; http://dx.doi.org/10.1016/j. cell.2006.07.029
71. Dudas A, Ahmad S, Gregan J. Sgo1 is required for cosegregation of sister chromatids during achiasmate meiosis I. Cell Cycle 2011; 10:951-5; PMID:21330786; http://dx.doi.org/10.4161/cc.10.6.15032
72. Hirose Y, Suzuki R, Ohba T, Hinohara Y, Matsuhara H, Yoshida M, et al. Chiasmata promote monopolar attachment of sister chromatids and their co-segregation toward the proper pole during meiosis I. PLoS Genet 2011; 7:e1001329; PMID:21423721; http://dx.doi.org/10.1371/journal.pgen.1001329
73. Sakuno T, Tanaka K, Hauf S, Watanabe Y. Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I. Dev Cell 2011; 21:534-45; PMID:21920317; http://dx.doi.org/10.1016/j.devcel. 2011.08.012
74. Ricke RM, Jeganathan KB, Malureanu L, Harrison AM, van Deursen JM. Bub1 kinase activity drives error correction and mitotic checkpoint control but not tumor suppression. J Cell Biol 2012; 199:931-49; PMID:23209306; http://dx.doi.org/10.1083/jcb.201205115
75. Li M, Guo H, Damuni Z. Purification and characterization of two potent heat-stable protein inhibitors of protein phosphatase 2A from bovine kidney. Biochemistry 1995; 34:1988-96; PMID:7531497; http://dx.doi.org/10.1021/ bi00006a020
76. Li M, Makkinje A, Damuni Z. The myeloid leukemiaassociated protein SET is a potent inhibitor of protein phosphatase 2A. J Biol Chem 1996; 271:11059-62; PMID:8626647; http://dx.doi.org/10.1074/jbc.271.19.11059
77. Herzog F, Kahraman A, Boehringer D, Mak R, Bracher A, Walzthoeni T, et al. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 2012; 337:1348-52; PMID:22984071; http://dx.doi.org/10.1126/science.1221483
78. Qi ST, Wang ZB, Ouyang YC, Zhang QH, Hu MW, Huang X, et al. Overexpression of SETβ, a protein localizing to centromeres, causes precocious separation of chromatids during the first meiosis of mouse oocyte. J Cell Sci 2013; PMID:23444375; http://dx.doi.org/10.1242/jcs.116541
79. Seo SB, McNamara P, Heo S, Turner A, Lane WS, Chakravarti D. Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 2001; 104:119-30; PMID:11163245; http://dx.doi.org/10.1016/S0092-8674(01)00196-9
80. Eot-Houllier G, Fulcrand G, Watanabe Y, Magnaghi-Jaulin L, Jaulin C. Histone deacetylase 3 is required for centromeric H3K4 deacetylation and sister chromatid cohesion. Genes Dev 2008; 22:2639-44; PMID:18832068; http://dx.doi.org/10.1101/gad.484108
81. Yang F, Baumann C, Viveiros MM, De La Fuente R. Histone hyperacetylation during meiosis interferes with large-scale chromatin remodeling, axial chromatid condensation and sister chromatid separation in the mammalian oocyte. Int J Dev Biol 2012; 56:889-99; PMID:23417411; http://dx.doi.org/10.1387/ijdb.120246rd
82. van den Berg IM, Eleveld C, van der Hoeven M, Birnie E, Steegers EA, Galjaard RJ, et al. Defective deacetylation of histone 4 K12 in human oocytes is associated with advanced maternal age and chromosome misalignment. Hum Reprod 2011; 26:1181-90; PMID:21349858; http://dx.doi.org/10.1093/humrep/der030
83. Akiyama T, Nagata M, Aoki F. Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. Proc Natl Acad Sci USA 2006; 103:7339-44; PMID:16651529; http://dx.doi.org/10.1073/pnas.0510946103
84. Okaz E, Argüello-Miranda O, Bogdanova A, Vinod PK, Lipp JJ, Markova Z, et al. Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/CAma1. Cell 2012; 151:603-18; PMID:23101628; http://dx.doi.org/10.1016/j.cell.2012.08.044
85. Sugimura I, Lilly MA. Bruno inhibits the expression of mitotic cyclins during the prophase I meiotic arrest of Drosophila oocytes. Dev Cell 2006; 10:127-35; PMID:16399084; http://dx.doi.org/10.1016/j.devcel.2005.10.018
86. Biedermann B, Wright J, Senften M, Kalchhauser I, Sarathy G, Lee MH, et al. Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 2009; 17:355-64; PMID:19758560; http://dx.doi.org/10.1016/j.devcel.2009.08.003
87. Miller MP, Unal E, Brar GA, Amon A. Meiosis I chromosome segregation is established through regulation of microtubule-kinetochore interactions. Elife 2012; 1:e00117; PMID:23275833; http://dx.doi.org/10.7554/eLife.00117
88. Carlile TM, Amon A. Meiosis I is established through division-specific translational control of a cyclin. Cell 2008; 133:280-91; PMID:18423199; http://dx.doi.org/10.1016/j.cell.2008.02.032
89. Touati SA, Cladière D, Lister LM, Leontiou I, Chambon JP, Rattani A, et al. Cyclin A2 is required for sister chromatid segregation, but not separase control, in mouse oocyte meiosis. Cell Rep 2012; 2:1077-87; PMID:23122964; http://dx.doi.org/10.1016/j.celrep.2012.10.002
90. Vasudevan NT, Mohan ML, Gupta MK, Hussain AK, Naga Prasad SV. Inhibition of protein phosphatase 2A activity by PI3Kγ regulates β-adrenergic receptor function. Mol Cell 2011; 41:636-48; PMID:21419339; http://dx.doi.org/ 10.1016/j.molcel.2011.02.025
91. Pagliuca FW, Collins MO, Lichawska A, Zegerman P, Choudhary JS, Pines J. Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol Cell 2011; 43:406-17; PMID:21816347; http://dx.doi.org/10.1016/j.molcel.2011.05.031
92. Adhikari D, Zheng W, Shen Y, Gorre N, Ning Y, Halet G, et al. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum Mol Genet 2012; 21:2476-84; PMID:22367880; http://dx.doi.org/10.1093/hmg/dds061
93. Merrick KA, Larochelle S, Zhang C, Allen JJ, Shokat KM, Fisher RP. Distinct activation pathways confer cyclin-binding specificity on Cdk1 and Cdk2 in human cells. Mol Cell 2008; 32:662-72; PMID:19061641; http://dx.doi.org/10. 1016/j.molcel.2008.10.022
94. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001; 2:280-91; PMID:11283700; http://dx.doi.org/10. 1038/35066065
95. De Souza E, Alberman E, Morris JK. Down syndrome and paternal age, a new analysis of casecontrol data collected in the 1960s. Am J Med Genet A 2009; 149A:1205-8; PMID:19449414; http://dx.doi.org/10.1002/ajmg.a.32850
96. Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, et al. Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 2010; 20:1511-21; PMID:20817533; http://dx.doi.org/10.1016/j.cub.2010.08.023
97. Liu L, Keefe DL. Defective cohesin is associated with agedependent misaligned chromosomes in oocytes. Reprod Biomed Online 2008; 16:103-12; PMID:18252055; http://dx.doi.org/10.1016/S1472-6483(10)60562-7
98. Daum JR, Potapova TA, Sivakumar S, Daniel JJ, Flynn JN, Rankin S, et al. Cohesion fatigue induces chromatid separation in cells delayed at metaphase. Curr Biol 2011; 21:1018-24; PMID:21658943; http://dx.doi.org/10.1016/j.cub.2011. 05.032
99. Wu JQ, Kornbluth S. Across the meiotic divide -CSF activity in the post-Emi2/XErp1 era. J Cell Sci 2008; 121:3509-14; PMID:18946022; http://dx.doi.org/10.1242/jcs.036855
100. Schmidt A, Rauh NR, Nigg EA, Mayer TU. Cytostatic factor: an activity that puts the cell cycle on hold. J Cell Sci 2006; 119:1213-8; PMID:16554437; http://dx.doi.org/10.1242/jcs.02919