Abstract
The generation of a viable, diploid organism depends on the formation of haploid gametes, oocytes, and spermatocytes, with the correct number of chromosomes. Halving the genome requires the execution of two consecutive specialized cell divisions named meiosis I and II. Unfortunately, and in contrast to male meiosis, chromosome segregation in oocytes is error prone, with human oocytes being extraordinarily “meiotically challenged”. Aneuploid oocytes, that are with the wrong number of chromosomes, give rise to aneuploid embryos when fertilized. In humans, most aneuploidies are lethal and result in spontaneous abortions. However, some trisomies survive to birth or even adulthood, such as the well-known trisomy 21, which gives rise to Down syndrome (Nagaoka et al. in Nat Rev Genet 13:493–504, 2012). A staggering 20–25 % of oocytes ready to be fertilized are aneuploid in humans. If this were not bad enough, there is an additional increase in meiotic missegregations as women get closer to menopause. A woman above 40 has a risk of more than 30 % of getting pregnant with a trisomic child. Worse still, in industrialized western societies, child birth is delayed, with women getting their first child later in life than ever. This trend has led to an increase of trisomic pregnancies by 70 % in the last 30 years (Nagaoka et al. in Nat Rev Genet 13:493–504, 2012; Schmidt et al. in Hum Reprod Update 18:29–43, 2012). To understand why errors occur so frequently during the meiotic divisions in oocytes, we review here the molecular mechanisms at works to control chromosome segregation during meiosis. An important mitotic control mechanism, namely the spindle assembly checkpoint or SAC, has been adapted to the special requirements of the meiotic divisions, and this review will focus on our current knowledge of SAC control in mammalian oocytes. Knowledge on how chromosome segregation is controlled in mammalian oocytes may help to identify risk factors important for questions related to human reproductive health.
Similar content being viewed by others
References
Almonacid M, Terret ME, Verlhac MH (2014) Actin-based spindle positioning: new insights from female gametes. J Cell Sci 127:477–483
Aravamudhan P, Goldfarb AA, Joglekar AP (2015) The kinetochore encodes a mechanical switch to disrupt spindle assembly checkpoint signalling. Nat Cell Biol 17:868–879
Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A, Kumar R, Jenkins RB, de Groen PC, Roche P, van Deursen JM (2004) BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 36:744–749
Balboula AZ, Schindler K (2014) Selective disruption of aurora C kinase reveals distinct functions from aurora B kinase during meiosis in mouse oocytes. PLoS Genet 10, e1004194
Batiha O, Swan A (2012) Evidence that the spindle assembly checkpoint does not regulate APC(Fzy) activity in Drosophila female meiosis. Genome / National Research Council Canada = Genome / Conseil national de recherches Canada 55:63–67
Buffin E, Emre D, Karess RE (2007) Flies without a spindle checkpoint. Nat Cell Biol 9:565–572
Chaigne A, Campillo C, Gov NS, Voituriez R, Sykes C, Verlhac MH, Terret ME (2015) A narrow window of cortical tension guides asymmetric spindle positioning in the mouse oocyte. Nat Commun 6:6027
Chambon JP, Hached K, Wassmann K (2013) Chromosome spreads with centromere staining in mouse oocytes. Methods Mol Biol 957:203–212
Chen RH, Waters JC, Salmon ED, Murray AW (1996) Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274:242–246
Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20:1522–1528
Collin P, Nashchekina O, Walker R, Pines J (2013) The spindle assembly checkpoint works like a rheostat rather than a toggle switch. Nat Cell Biol 15:1378–1385
Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, Cooke HJ, Stewart AF, Wassmann K, Jasin M, Keeney S, Toth A (2011) Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13:599–610
Danylevska A, Kovacovicova K, Awadova T, Anger M (2014) The frequency of precocious segregation of sister chromatids in mouse female meiosis I is affected by genetic background. Chromosome Res 22:365–373
Darribère T (2003) Le développement d’un mammifère : la souris. Belin 19–71
Davie E (2012) A first child at 28 years old. Insee 1419
Davydenko O, Schultz RM, Lampson MA (2013) Increased CDK1 activity determines the timing of kinetochore-microtubule attachments in meiosis I. J Cell Biol 202:221–229
Dick AE, Gerlich DW (2013) Kinetic framework of spindle assembly checkpoint signalling. Nat Cell Biol 15:1370–1377
Duncan FE, Chiang T, Schultz RM, Lampson MA (2009) Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol Reprod 81:768–776
Felix MA, Labbe JC, Doree M, Hunt T, Karsenti E (1990) Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature 346:379–382
Fernandez-Miranda G, Trakala M, Martin J, Escobar B, Gonzalez A, Ghyselinck NB, Ortega S, Canamero M, Perez de Castro I, Malumbres M (2011) Genetic disruption of aurora B uncovers an essential role for aurora C during early mammalian development. Development 138:2661–2672
Foijer F, Xie SZ, Simon JE, Bakker PL, Conte N, Davis SH, Kregel E, Jonkers J, Bradley A, Sorger PK (2014) Chromosome instability induced by Mps1 and p53 mutation generates aggressive lymphomas exhibiting aneuploidy-induced stress. Proc Natl Acad Sci U S A 111:13427–13432
Foley EA, Kapoor TM (2013) Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 14:25–37
Gemzell CA (1962) Induction of ovulation with human pituitary gonadotrophins. Fertil Steril 13:153–168
Gomez R, Valdeolmillos A, Parra MT, Viera A, Carreiro C, Roncal F, Rufas JS, Barbero JL, Suja JA (2007) Mammalian SGO2 appears at the inner centromere domain and redistributes depending on tension across centromeres during meiosis II and mitosis. EMBO Rep 8:173–180
Gorr IH, Reis A, Boos D, Wuhr M, Madgwick S, Jones KT, Stemmann O (2006) Essential CDK1-inhibitory role for separase during meiosis I in vertebrate oocytes. Nat Cell Biol 8:1035–1037
Gui L, Homer H (2012) Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development 139:1941–1946
Hached K, Xie SZ, Buffin E, Cladiere D, Rachez C, Sacras M, Sorger PK, Wassmann K (2011) Mps1 at kinetochores is essential for female mouse meiosis I. Development 138:2261–2271
Handyside AH (2012) Molecular origin of female meiotic aneuploidies. Biochim Biophys Acta 1822:1913–1920
Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280–291
Hassold T, Abruzzo M, Adkins K, Griffin D, Merrill M, Millie E, Saker D, Shen J, Zaragoza M (1996) Human aneuploidy: incidence, origin, and etiology. Environ Mol Mutagen 28:167–175
Hauf S (2013) The spindle assembly checkpoint: progress and persistent puzzles. Biochem Soc Trans 41:1755–1760
Hiruma Y, Sacristan C, Pachis ST, Adamopoulos A, Kuijt T, Ubbink M, von Castelmur E, Perrakis A, Kops GJ (2015) CELL DIVISION CYCLE. Competition between MPS1 and microtubules at kinetochores regulates spindle checkpoint signaling. Science 348:1264–1267
Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M (2005a) Mad2 is required for inhibiting securin and cyclin B degradation following spindle depolymerisation in meiosis I mouse oocytes. Reproduction 130:829–843
Homer HA, McDougall A, Levasseur M, Yallop K, Murdoch AP, Herbert M (2005b) Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securin during meiosis I in mouse oocytes. Genes Dev 19:202–207
Homer H, Gui L, Carroll J (2009) A spindle assembly checkpoint protein functions in prophase I arrest and prometaphase progression. Science 326:991–994
Ishiguro T, Tanaka K, Sakuno T, Watanabe Y (2010) Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 12:500–506
Jeganathan KB, van Deursen JM (2006) Differential mitotic checkpoint protein requirements in somatic and germ cells. Biochem Soc Trans 34:583–586
Ji Z, Gao H, Yu H (2015) CELL DIVISION CYCLE. Kinetochore attachment sensed by competitive Mps1 and microtubule binding to Ndc80C. Science 348:1260–1264
Jones KT, Lane SI (2013) Molecular causes of aneuploidy in mammalian eggs. Development 140:3719–3730
Kabeche L, Compton DA (2013) Cyclin A regulates kinetochore microtubules to promote faithful chromosome segregation. Nature 502:110–113
Katis VL, Lipp JJ, Imre R, Bogdanova A, Okaz E, Habermann B, Mechtler K, Nasmyth K, Zachariae W (2010) Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 18:397–409
Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y (2010) Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327:172–177
Kim J, Ishiguro K, Nambu A, Akiyoshi B, Yokobayashi S, Kagami A, Ishiguro T, Pendas AM, Takeda N, Sakakibara Y, Kitajima TS, Tanno Y, Sakuno T, Watanabe Y (2015) Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature 517:466–471
Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441:46–52
Kitajima TS, Ohsugi M, Ellenberg J (2011) Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146:568–581
Kolano A, Brunet S, Silk AD, Cleveland DW, Verlhac MH (2012) Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc Natl Acad Sci U S A 109:E1858–E1867
Kouznetsova A, Lister L, Nordenskjold M, Herbert M, Hoog C (2007) Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat Genet 39:966–968
Kouznetsova A, Hernandez-Hernandez A, Hoog C (2014) Merotelic attachments allow alignment and stabilization of chromatids in meiosis II oocytes. Nat Commun 5:4409
Kruse T, Zhang G, Larsen MS, Lischetti T, Streicher W, Kragh Nielsen T, Bjorn SP, Nilsson J (2013) Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J Cell Sci 126:1086–1092
Lane SI, Jones KT (2014) Non-canonical function of spindle assembly checkpoint proteins after APC activation reduces aneuploidy in mouse oocytes. Nat Commun 5:3444
Lane SI, Chang HY, Jennings PC, Jones KT (2010) The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint. Reproduction 140:521–530
Lane SI, Yun Y, Jones KT (2012) Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development 139:1947–1955
Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 10:42–52
Leland S, Nagarajan P, Polyzos A, Thomas S, Samaan G, Donnell R, Marchetti F, Venkatachalam S (2009) Heterozygosity for a Bub1 mutation causes female-specific germ cell aneuploidy in mice. Proc Natl Acad Sci U S A 106:12776–12781
LeMaire-Adkins R, Radke K, Hunt PA (1997) Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J Cell Biol 139:1611–1619
Li R, Albertini DF (2013) The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nature Rev 14:141–152
Li M, Li S, Yuan J, Wang ZB, Sun SC, Schatten H, Sun QY (2009) Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. PLoS One 4, e7701
Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, Jessberger R, Kirkwood TB, Hoog C, Herbert M (2010) Age-related meiotic segregation errors in Mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20:1511–1521
Liu L, Keefe DL (2002) Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice. Hum Reprod 17:2678–2685
Liu D, Vader G, Vromans MJ, Lampson MA, Lens SM (2009) Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323:1350–1353
Liu D, Shao H, Wang H, Liu XJ (2014) Meiosis I in Xenopus oocytes is not error-prone despite lacking spindle assembly checkpoint. Cell Cycle 13:1602–1606
Llano E, Gomez R, Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Vazquez-Quinones L, Hernandez T, de Alava E, Cuadrado A, Barbero JL, Suja JA, Pendas AM (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22:2400–2413
London N, Biggins S (2014) Signalling dynamics in the spindle checkpoint response. Nat Rev Mol Cell Biol 15:736–747
Luo X, Tang Z, Rizo J, Yu H (2002) The mad2 spindle checkpoint protein undergoes similar major conformational changes upon binding to either mad1 or cdc20. Mol Cell 9:59–71
Maciejowski J, George KA, Terret ME, Zhang C, Shokat KM, Jallepalli PV (2010) Mps1 directs the assembly of Cdc20 inhibitory complexes during interphase and mitosis to control M phase timing and spindle checkpoint signaling. J Cell Biol 190:89–100
Madgwick S, Hansen DV, Levasseur M, Jackson PK, Jones KT (2006) Mouse Emi2 is required to enter meiosis II by reestablishing cyclin B1 during interkinesis. J Cell Biol 174:791–801
Maiato H, DeLuca J, Salmon ED, Earnshaw WC (2004) The dynamic kinetochore-microtubule interface. J Cell Sci 117:5461–5477
McGuinness BE, Anger M, Kouznetsova A, Gil-Bernabe AM, Helmhart W, Kudo NR, Wuensche A, Taylor S, Hoog C, Novak B, Nasmyth K (2009) Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol 19:369–380
Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7:45–60
Merriman JA, Lane SI, Holt JE, Jennings PC, Garcia-Higuera I, Moreno S, McLaughlin EA, Jones KT (2013) Reduced chromosome cohesion measured by interkinetochore distance is associated with aneuploidy even in oocytes from young mice. Biol Reprod 88:31
Michel LS, Liberal V, Chatterjee A, Kirchwegger R, Pasche B, Gerald W, Dobles M, Sorger PK, Murty VVVS, Benezra R (2001) MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409:355–359
Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8:379–393
Nagaoka SI, Hodges CA, Albertini DF, Hunt PA (2011) Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr Biol 21:651–657
Nagaoka SI, Hassold TJ, Hunt PA (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13:493–504
Nguyen AL, Gentilello AS, Balboula AZ, Shrivastava V, Ohring J, Schindler K (2014) Phosphorylation of threonine 3 on histone H3 by haspin kinase is required for meiosis I in mouse oocytes. J Cell Sci 127:5066–5078
Niault T, Hached K, Sotillo R, Sorger PK, Maro B, Benezra R, Wassmann K (2007) Changing Mad2 levels affects chromosome segregation and spindle assembly checkpoint control in female mouse meiosis I. PLoS One 2, e1165
Nijenhuis W, Vallardi G, Teixeira A, Kops GJ, Saurin AT (2014) Negative feedback at kinetochores underlies a responsive spindle checkpoint signal. Nat Cell Biol 16:1257–1264
O’Connell CB, Loncarek J, Hergert P, Kourtidis A, Conklin DS, Khodjakov A (2008) The spindle assembly checkpoint is satisfied in the absence of interkinetochore tension during mitosis with unreplicated genomes. J Cell Biol 183:29–36
Peters JM, Tedeschi A, Schmitz J (2008) The cohesin complex and its roles in chromosome biology. Genes Dev 22:3089–3114
Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440
Pinsky BA, Biggins S (2005) The spindle checkpoint: tension versus attachment. Trends Cell Biol 15:486–493
Rattani A, Wolna M, Ploquin M, Helmhart W, Morrone S, Mayer B, Godwin J, Xu W, Stemmann O, Pendas A, Nasmyth K (2013) Sgol2 provides a regulatory platform that coordinates essential cell cycle processes during meiosis I in oocytes. eLife 2, e01133
Rattani A, Vinod PK, Godwin J, Tachibana-Konwalski K, Wolna M, Malumbres M, Novak B, Nasmyth K (2014) Dependency of the spindle assembly checkpoint on Cdk1 renders the anaphase transition irreversible. Curr Biol 24:630–637
Ricke RM, Jeganathan KB, Malureanu L, Harrison AM, van Deursen JM (2012) Bub1 kinase activity drives error correction and mitotic checkpoint control but not tumor suppression. J Cell Biol 199:931–949
Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441:53–61
Rieder CL, Cole RW, Khodjakov A, Sluder G (1995) The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130:941–948
Riris S, Webster P, Homer H (2014) Digital multiplexed mRNA analysis of functionally important genes in single human oocytes and correlation of changes in transcript levels with oocyte protein expression. Fertil Steril 101:857–864
Rodriguez-Bravo V, Maciejowski J, Corona J, Buch HK, Collin P, Kanemaki MT, Shah JV, Jallepalli PV (2014) Nuclear pores protect genome integrity by assembling a premitotic and Mad1-dependent anaphase inhibitor. Cell 156:1017–1031
Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157:219–229
Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, Riedel CG, Ammerer G, Mechtler K, Gregan J (2010) Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 9:2657–2662
Sacristan C, Kops GJ (2015) Joined at the hip: kinetochores, microtubules, and spindle assembly checkpoint signaling. Trends Cell Biol 25:21–28
Santaguida S, Tighe A, D’Alise AM, Taylor SS, Musacchio A (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J Cell Biol 190:73–87
Sasai K, Katayama H, Stenoien DL, Fujii S, Honda R, Kimura M, Okano Y, Tatsuka M, Suzuki F, Nigg EA, Earnshaw WC, Brinkley WR, Sen S (2004) Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil Cytoskeleton 59:249–263
Sebestova J, Danylevska A, Novakova L, Kubelka M, Anger M (2012) Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle 11:3011–3018
Severson AF, Meyer BJ (2014) Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes. eLife 3, e03467
Severson AF, Ling L, van Zuylen V, Meyer BJ (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev 23:1763–1778
Shao H, Li R, Ma C, Chen E, Liu XJ (2013) Xenopus oocyte meiosis lacks spindle assembly checkpoint control. J Cell Biol 201:191–200
Siomos MF, Badrinath A, Pasierbek P, Livingstone D, White J, Glotzer M, Nasmyth K (2001) Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Curr Biol 11:1825–1835
Slattery SD, Moore RV, Brinkley BR, Hall RM (2008) Aurora-C and Aurora-B share phosphorylation and regulation of CENP-A and Borealin during mitosis. Cell Cycle 7:787–795
Slattery SD, Mancini MA, Brinkley BR, Hall RM (2009) Aurora-C kinase supports mitotic progression in the absence of Aurora-B. Cell Cycle 8:2984–2994
Stukenberg PT, Burke DJ (2015) Connecting the microtubule attachment status of each kinetochore to cell cycle arrest through the spindle assembly checkpoint. Chromosoma
Suijkerbuijk SJ, Vleugel M, Teixeira A, Kops GJ (2012) Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev Cell 23:745–755
Sullivan M, Morgan DO (2007) Finishing mitosis, one step at a time. Nat Rev Mol Cell Biol 8:894–903
Sun SC, Kim NH (2012) Spindle assembly checkpoint and its regulators in meiosis. Hum Reprod Update 18:60–72
Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, Adams DJ, Nasmyth K (2010) Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 24:2505–2516
Tachibana-Konwalski K, Godwin J, Borsos M, Rattani A, Adams DJ, Nasmyth K (2013) Spindle assembly checkpoint of oocytes depends on a kinetochore structure determined by cohesin in meiosis I. Curr Biol 23:2534–2539
Tang Z, Bharadwaj R, Li B, Yu H (2001) Mad2-Independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev Cell 1:227–237
Tang CJ, Lin CY, Tang TK (2006) Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis. Dev Biol 290:398–410
Terret ME, Wassmann K (2008) Meiotic weakness : the first division. Med Sci (Paris) 24:197–204
Touati SA, Cladiere D, Lister LM, Leontiou I, Chambon JP, Rattani A, Bottger F, Stemmann O, Nasmyth K, Herbert M, Wassmann K (2012) Cyclin A2 Is required for sister chromatid segregation, but not separase control, in mouse oocyte meiosis. Cell Rep
Touati SA, Buffin E, Cladiere D, Hached K, Rachez C, van Deursen JM, Wassmann K (2015) Mouse oocytes depend on BubR1 for proper chromosome segregation but not for prophase I arrest. Nat Commun 6:6946
Tsurumi C, Hoffmann S, Geley S, Graeser R, Polanski Z (2004) The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J Cell Biol 167:1037–1050
Tunquist BJ, Schwab MS, Chen LG, Maller JL (2002) The spindle checkpoint kinase bub1 and cyclin e/cdk2 both contribute to the establishment of meiotic metaphase arrest by cytostatic factor. Curr Biol 12:1027–1033
Tunquist BJ, Eyers PA, Chen LG, Lewellyn AL, Maller JL (2003) Spindle checkpoint proteins Mad1 and Mad2 are required for cytostatic factor-mediated metaphase arrest. J Cell Biol 163:1231–1242
Uhlmann F (2003) Chromosome cohesion and separation: from men and molecules. Curr Biol 13:R104–R114
van der Waal MS, Hengeveld RC, van der Horst A, Lens SM (2012) Cell division control by the chromosomal passenger complex. Exp Cell Res 318:1407–1420
Vera M, Peinado V, Al-Asmar N, Gruhn J, Rodrigo L, Hassold T, Rubio C (2012) Human male meiosis and sperm aneuploidies. InTech, Bookchapter in The causes and consequences of aneuploidy in eukaryotic cells (Editor: Z. Storchova)
Vleugel M, Hoogendoorn E, Snel B, Kops GJ (2012) Evolution and function of the mitotic checkpoint. Dev Cell 23:239–250
Wang JY, Lei ZL, Nan CL, Yin S, Liu J, Hou Y, Li YL, Chen DY, Sun QY (2007) RNA Interference as a tool to study the function of MAD2 in mouse oocyte meiotic maturation. Mol Reprod Dev 74:116–124
Wassmann K (2013) Sister chromatid segregation in meiosis II: deprotection through phosphorylation. Cell Cycle 12:1352–1359
Wassmann K, Benezra R (1998) Mad2 transiently associates with an APC/p55Cdc complex during mitosis. Proc Natl Acad Sci U S A 95:11193–11198
Wassmann K, Liberal V, Benezra R (2003a) Mad2 phosphorylation regulates its association with Mad1 and the APC/C. EMBO J 22:797–806
Wassmann K, Niault T, Maro B (2003b) Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 13:1596–1608
Watanabe Y (2012) Geometry and force behind kinetochore orientation: lessons from meiosis. Nat Rev Mol Cell Biol 13:370–382
Wei L, Liang XW, Zhang QH, Li M, Yuan J, Li S, Sun SC, Ouyang YC, Schatten H, Sun QY (2009) BubR1 is a spindle assembly checkpoint protein regulating meiotic cell cycle progression of mouse oocyte. Cell cycle Georgetown: 1112–1121
Woods LM, Hodges CA, Baart E, Baker SM, Liskay M, Hunt PA (1999) Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J Cell Biol 145:1395–1406
Wu JQ, Kornbluth S (2008) Across the meiotic divide—CSF activity in the post-Emi2/XErp1 era. J Cell Sci 121:3509–3514
Yang Q, Ferrell JE Jr (2013) The Cdk1-APC/C cell cycle oscillator circuit functions as a time-delayed, ultrasensitive switch. Nat Cell Biol 15:519–525
Yang KT, Li SK, Chang CC, Tang CJ, Lin YN, Lee SC, Tang TK (2010) Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol Biol Cell 21:2371–2383
Yin S, Wang Q, Liu JH, Ai JS, Liang CG, Hou Y, Chen DY, Schatten H, Sun QY (2006) Bub1 prevents chromosome misalignment and precocious anaphase during mouse oocyte meiosis. Cell Cycle 5:2130–2137
Yun Y, Lane SI, Jones KT (2014) Premature dyad separation in meiosis II is the major segregation error with maternal age in mouse oocytes. Development 141:199–208
Zhang D, Li M, Ma W, Hou Y, Li YH, Li SW, Sun QY, Wang WH (2005) Localization of mitotic arrest deficient 1 (MAD1) in mouse oocytes during the first meiosis and its functions as a spindle checkpoint protein. Biol Reprod 72:58–68
Acknowledgments
Work in the lab of K. Wassmann is supported by a grant from the Agence Nationale de la Recherche (ANR-12-BSV2-0005-01), the Centre National de la Recherche Scientifique (CNRS), and Université Paris 6. We thank E. Buffin, A. Vallot, and W. El Yakoubi for discussion and comments on the manuscript.
Conflict of interest
The authors declare that they have no conflict of interest. For this review article, no studies with human participants or animals were performed by any of the authors.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is part of a Special Issue on “Recent advances in meiotic chromosome structure, recombination and segregation” edited by Marco Barchi, Paula Cohen and Scott Keeney.
Rights and permissions
About this article
Cite this article
Touati, S.A., Wassmann, K. How oocytes try to get it right: spindle checkpoint control in meiosis. Chromosoma 125, 321–335 (2016). https://doi.org/10.1007/s00412-015-0536-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-015-0536-7