Abstract
Chromosome segregation in mammalian oocytes is prone to errors causing aneuploidy with consequences such as precocious termination of development or severe developmental disorders. Aneuploidy also represents a serious problem in procedures utilizing mammalian gametes and early embryos in vitro. In our study, we focused on congression defects during meiosis I and observed whole nondisjoined bivalents in meiosis II as a direct consequence, together with a substantially delayed first polar body extrusion. We also show that the congression defects are accompanied by less stable attachments of the kinetochores. Our results describe a process by which congression defects directly contribute to aneuploidy.
References
1.
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 20:1522-1528 (2010).
2.
Chmátal L, Gabriel SI, Mitsainas GP, Martínez-Vargas J, Ventura J, et al: Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr Biol 24:2295-2300 (2014).
3.
Chmátal L, Yang K, Schultz RM, Lampson MA: Spatial regulation of kinetochore microtubule attachments by destabilization at spindle poles in meiosis I. Curr Biol 25:1835-1841 (2015).
4.
Collins J, Jones KT: DNA damage responses in mammalian oocytes. Reproduction 152:R15-R22 (2016).
5.
Danadova J, Matijescukova N, Danylevska AM, Anger M: Increased frequency of chromosome congression defects and aneuploidy in mouse oocytes cultured at lower temperature. Reprod Fertil Dev DOI: 10.1071/RD1530 (2016).
6.
Eichenlaub-Ritter U: Oocyte ageing and its cellular basis. Int J Dev Biol 56:841-852 (2012).
7.
Hassold T, Hunt P: To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280-291 (2001).
8.
Herbert M, Kalleas D, Cooney D, Lamb M, Lister L: Meiosis and maternal aging: insights from aneuploid oocytes and trisomy births. Cold Spring Harb Perspect Biol 7:a017970 (2015).
9.
Holt JE, Lane SI, Jennings P, García-Higuera I, Moreno S, Jones KT: APC (FZR1) prevents nondisjunction in mouse oocytes by controlling meiotic spindle assembly timing. Mol Biol Cell 23:3970-3981 (2012).
10.
Hornak M, Jeseta M, Musilova P, Pavlok A, Kubelka M, et al: Frequency of aneuploidy related to age in porcine oocytes. PLoS One 6:e18892 (2011).
11.
Ishiguro T, Tanaka K, Sakuno T, Watanabe Y: Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 12:500-506 (2010).
12.
Jones KT, Lane SI: Molecular causes of aneuploidy in mammalian eggs. Development 140:3719-3730 (2013).
13.
Katis VL, Lipp JJ, Imre R, Bogdanova A, Okaz E, et al: Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 18:397-409 (2010).
14.
Kovacovicova K, Awadova T, Mikel P, Anger M: In vitro maturation of mouse oocytes increases the level of Kif11/Eg5 on meiosis II spindles. Biol Reprod 95:18 (2016).
15.
Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, et al: Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 126:135-146 (2006).
16.
Kudo NR, Anger M, Peters AH, Stemmann O, Theussl HC, et al: Role of cleavage by separase of the Rec8 kleisin subunit of cohesin during mammalian meiosis I. J Cell Sci 122:2686-2698 (2009).
17.
Lane SI, Yun Y, Jones KT: 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 (2012).
18.
Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, et al: Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20:1511-1521 (2010).
19.
Mailhes JB: Faulty spindle checkpoint and cohesion protein activities predispose oocytes to premature chromosome separation and aneuploidy. Environ Mol Mutagen 49:642-658 (2008).
20.
Nagaoka SI, Hassold TJ, Hunt PA: Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13:493-504 (2012).
21.
Petronczki M, Siomos MF, Nasmyth K: Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423-440 (2003).
22.
Phadnis N, Cipak L, Polakova S, Hyppa RW, Cipakova I, et al: Casein kinase 1 and phosphorylation of cohesin subunit Rec11 (SA3) promote meiotic recombination through linear element formation. PLoS Genet 11: e1005225 (2015).
23.
Revenkova E, Herrmann K, Adelfalk C, Jessberger R: Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20:1529-1533 (2010).
24.
Rumpf C, Cipak L, Dudas A, Benko Z, Pozgajova M, et al: Casein kinase 1 is required for efficient removal of Rec8 during meiosis I. Cell Cycle 9:2657-2662 (2010).
25.
Sebestova J, Danylevska A, Novakova L, Kubelka M, Anger M: Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle 11:3011-3018 (2012).
26.
Simunić J, Tolić IM: Mitotic spindle assembly: building the bridge between sister K-fibers. Trends Biochem Sci 41:824-833 (2016).
27.
Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, et al: Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 24:2505-2516 (2010).
28.
Touati SA, Wassmann K: How oocytes try to get it right: spindle checkpoint control in meiosis. Chromosoma 125:321-335 (2015).
29.
Tsutsumi M, Fujiwara R, Nishizawa H, Ito M, Kogo H, et al: Age-related decrease of meiotic cohesins in human oocytes. PLoS One 9:e96710 (2014).
© 2017 S. Karger AG, Basel
2017
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