Meiosis I in Xenopus Oocytes is Not Error-prone Despite Lacking Spindle Assembly Checkpoint

Overview

Journal Cell Cycle

Specialty Cell Biology

Date 2014 Mar 21

PMID 24646611

Citations 7

Authors

Dandan Liu

Hua Shao

Hongmei Wang

X Johne Liu

Affiliations

Soon will be listed here.

Abstract

The spindle assembly checkpoint, SAC, is a surveillance mechanism to control the onset of anaphase during cell division. SAC prevents anaphase initiation until all chromosome pairs have achieved bipolar attachment and aligned at the metaphase plate of the spindle. In doing so, SAC is thought to be the key mechanism to prevent chromosome nondisjunction in mitosis and meiosis. We have recently demonstrated that Xenopus oocyte meiosis lacks SAC control. This prompted the question of whether Xenopus oocyte meiosis is particularly error-prone. In this study, we have karyotyped a total of 313 Xenopus eggs following in vitro oocyte maturation. We found no hyperploid egg, out of 204 metaphase II eggs with countable chromosome spreads. Therefore, chromosome nondisjunction is very rare during Xenopus oocyte meiosis I, despite the lack of SAC.

Citing Articles

Distinct checkpoint and homolog biorientation pathways regulate meiosis I in Drosophila oocytes.

Shapiro J, Changela N, Jang J, Joshi J, McKim K PLoS Genet. 2025; 21(1):e1011400.

PMID: 39879252 PMC: 11809923. DOI: 10.1371/journal.pgen.1011400.

Distinct checkpoint and homolog biorientation pathways regulate meiosis I in oocytes.

Shapiro J, Changela N, Jang J, Joshi J, McKim K bioRxiv. 2024; .

PMID: 39229242 PMC: 11370425. DOI: 10.1101/2024.08.21.608908.

Selfish centromeres and the wastefulness of human reproduction.

Hurst L PLoS Biol. 2022; 20(7):e3001671.

PMID: 35788750 PMC: 9255743. DOI: 10.1371/journal.pbio.3001671.

Meiotic spindle assembly checkpoint and aneuploidy in males versus females.

Lane S, Kauppi L Cell Mol Life Sci. 2018; 76(6):1135-1150.

PMID: 30564841 PMC: 6513798. DOI: 10.1007/s00018-018-2986-6.

Living Xenopus oocytes, eggs, and embryos as models for cell division.

Varjabedian A, Kita A, Bement W Methods Cell Biol. 2018; 144:259-285.

PMID: 29804672 PMC: 6050073. DOI: 10.1016/bs.mcb.2018.03.013.

References

Zhang X, Ma C, Miller A, Katbi H, Bement W, Liu X . Polar body emission requires a RhoA contractile ring and Cdc42-mediated membrane protrusion. Dev Cell. 2008; 15(3):386-400. PMC: 3549423. DOI: 10.1016/j.devcel.2008.07.005. View

Schuh M, Ellenberg J . Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007; 130(3):484-98. DOI: 10.1016/j.cell.2007.06.025. View

Ohi R, Burbank K, Liu Q, Mitchison T . Nonredundant functions of Kinesin-13s during meiotic spindle assembly. Curr Biol. 2007; 17(11):953-9. DOI: 10.1016/j.cub.2007.04.057. View

Chang C, Nagy Z, Abdelmassih R, Liu J, Yang X, Tian X . Interactions of the meiotic spindle with mitotic chromosomes in GV mouse oocytes. Reprod Biomed Online. 2006; 13(2):213-21. DOI: 10.1016/s1472-6483(10)60618-9. View

Chiang T, Duncan F, Schindler K, Schultz R, Lampson M . Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol. 2010; 20(17):1522-8. PMC: 2939204. DOI: 10.1016/j.cub.2010.06.069. View

Liu X . Polar body emission. Cytoskeleton (Hoboken). 2012; 69(10):670-85. DOI: 10.1002/cm.21041. View

Kuliev A, Zlatopolsky Z, Kirillova I, Spivakova J, Cieslak Janzen J . Meiosis errors in over 20,000 oocytes studied in the practice of preimplantation aneuploidy testing. Reprod Biomed Online. 2010; 22(1):2-8. DOI: 10.1016/j.rbmo.2010.08.014. View

Kudo N, Wassmann K, Anger M, Schuh M, Wirth K, Xu H . Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell. 2006; 126(1):135-46. DOI: 10.1016/j.cell.2006.05.033. View

Kitajima T, Ohsugi M, Ellenberg J . Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell. 2011; 146(4):568-81. DOI: 10.1016/j.cell.2011.07.031. View

10.

Angell R . Predivision in human oocytes at meiosis I: a mechanism for trisomy formation in man. Hum Genet. 1991; 86(4):383-7. DOI: 10.1007/BF00201839. View

11.

Murray A, Kirschner M . Dominoes and clocks: the union of two views of the cell cycle. Science. 1989; 246(4930):614-21. DOI: 10.1126/science.2683077. View

12.

Houghtaling B, Yang G, Matov A, Danuser G, Kapoor T . Op18 reveals the contribution of nonkinetochore microtubules to the dynamic organization of the vertebrate meiotic spindle. Proc Natl Acad Sci U S A. 2009; 106(36):15338-43. PMC: 2741252. DOI: 10.1073/pnas.0902317106. View

13.

Davydenko O, Schultz R, Lampson M . Increased CDK1 activity determines the timing of kinetochore-microtubule attachments in meiosis I. J Cell Biol. 2013; 202(2):221-9. PMC: 3718970. DOI: 10.1083/jcb.201303019. View

14.

Shao H, Ma C, Zhang X, Li R, Miller A, Bement W . Aurora B regulates spindle bipolarity in meiosis in vertebrate oocytes. Cell Cycle. 2012; 11(14):2672-80. PMC: 3409009. DOI: 10.4161/cc.21016. View

15.

Hached K, Xie S, Buffin E, Cladiere D, Rachez C, Sacras M . Mps1 at kinetochores is essential for female mouse meiosis I. Development. 2011; 138(11):2261-71. DOI: 10.1242/dev.061317. View

16.

Koehler K, Schrump S, Cherry J, Hassold T, Hunt P . Near-human aneuploidy levels in female mice with homeologous chromosomes. Curr Biol. 2006; 16(15):R579-80. DOI: 10.1016/j.cub.2006.07.018. View

17.

Kalt M, Gall J . Observations on early germ cell development and premeiotic ribosomal DNA amplification in Xenopus laevis. J Cell Biol. 1974; 62(2):460-72. PMC: 2109412. DOI: 10.1083/jcb.62.2.460. View

18.

Hodges C, Hunt P . Simultaneous analysis of chromosomes and chromosome-associated proteins in mammalian oocytes and embryos. Chromosoma. 2002; 111(3):165-9. DOI: 10.1007/s00412-002-0195-3. View

19.

McGuinness B, Anger M, Kouznetsova A, Gil-Bernabe A, Helmhart W, Kudo N . Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol. 2009; 19(5):369-80. DOI: 10.1016/j.cub.2009.01.064. View

20.

Lister L, Kouznetsova A, Hyslop L, Kalleas D, Pace S, Barel J . Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol. 2010; 20(17):1511-21. DOI: 10.1016/j.cub.2010.08.023. View