Effects of Post-ovulatory Aging on Centromeric Cohesin Protection in Murine MII Oocytes

Overview

Journal Reprod Med Biol

Specialty Biology

Date 2022 Apr 7

PMID 35386382

Authors

Gaku Shimoi

Rico Wakabayashi

Ryu Ishikawa

Yuichi Kameyama

Affiliations

Soon will be listed here.

Abstract

Purpose: Post-ovulatory aging causes a high frequency of aneuploidy during meiosis II in mouse oocytes, irrespective of maternal age. In this study, we evaluated the effects of post-ovulatory oocyte aging on the protection of chromosomal cohesion involved in aneuploidy and verified the relationship between PP2A or SGO2 expression and the phosphorylation level of REC8 in oocytes.

Methods: Murine ovulated oocytes were incubated for 6 or 12 h after collection and denoted as the aged group. The oocytes examined immediately after collection were used as the control group. Immunofluorescent staining was used to detect the localization of PP2A, SGO2, BUB1, AURORA B, and MAD2 in the chromosomal centromere. Immunoblotting was used to quantify the expression of proteins describe above and REC8 in the oocytes.

Results: PP2A expression involved in the de-phosphorylation of REC8 decreased over time in oocytes, suggesting a deficiency in PP2A in centromeres. This indicated an increase in the level of phosphorylated REC8, which destabilizes centromeric cohesion in oocytes. In contrast, SGO2 expression was significantly high in aged oocytes.

Conclusions: The findings show that post-ovulatory aging destabilizes the centromeric cohesin protection in oocytes and can cause aneuploidy, which is often observed in aged oocytes during meiosis II.

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References

Nagy Z, Rienzi L, Ubaldi F, Greco E, Massey J, Kort H . Effect of reduced oocyte aging on the outcome of rescue intracytoplasmic sperm injection. Fertil Steril. 2006; 85(4):901-6. DOI: 10.1016/j.fertnstert.2005.09.029. View

Asai Y, Fukuchi K, Tanno Y, Koitabashi-Kiyozuka S, Kiyozuka T, Noda Y . Aurora B kinase activity is regulated by SET/TAF1 on Sgo2 at the inner centromere. J Cell Biol. 2019; 218(10):3223-3236. PMC: 6781429. DOI: 10.1083/jcb.201811060. View

Franasiak J, Forman E, Hong K, Werner M, Upham K, Treff N . Aneuploidy across individual chromosomes at the embryonic level in trophectoderm biopsies: changes with patient age and chromosome structure. J Assist Reprod Genet. 2014; 31(11):1501-9. PMC: 4389946. DOI: 10.1007/s10815-014-0333-x. View

Sun S, Kim N . Spindle assembly checkpoint and its regulators in meiosis. Hum Reprod Update. 2011; 18(1):60-72. DOI: 10.1093/humupd/dmr044. View

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

Jones K . Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum Reprod Update. 2007; 14(2):143-58. DOI: 10.1093/humupd/dmm043. View

Garcia-Cruz R, Brieno M, Roig I, Grossmann M, Velilla E, Pujol A . Dynamics of cohesin proteins REC8, STAG3, SMC1 beta and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes. Hum Reprod. 2010; 25(9):2316-27. DOI: 10.1093/humrep/deq180. 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

Steuerwald N, Cohen J, Herrera R, Sandalinas M, Brenner C . Association between spindle assembly checkpoint expression and maternal age in human oocytes. Mol Hum Reprod. 2001; 7(1):49-55. DOI: 10.1093/molehr/7.1.49. View

10.

Hassold T, Hunt P . To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet. 2001; 2(4):280-91. DOI: 10.1038/35066065. View

11.

Duncan F, Hornick J, Lampson M, Schultz R, Shea L, Woodruff T . Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell. 2012; 11(6):1121-4. PMC: 3491123. DOI: 10.1111/j.1474-9726.2012.00866.x. View

12.

Kitajima T, Kawashima S, Watanabe Y . The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature. 2004; 427(6974):510-7. DOI: 10.1038/nature02312. View

13.

Hu M, Wang Z, Jiang Z, Qi S, Huang L, Liang Q . Scaffold subunit Aalpha of PP2A is essential for female meiosis and fertility in mice. Biol Reprod. 2014; 91(1):19. DOI: 10.1095/biolreprod.114.120220. View

14.

Miao Y, Kikuchi K, Sun Q, Schatten H . Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009; 15(5):573-85. DOI: 10.1093/humupd/dmp014. View

15.

Ohama T . [Targeting PP2A inhibitors as a novel anti-cancer strategy ]. Nihon Yakurigaku Zasshi. 2015; 145(6):293-8. DOI: 10.1254/fpj.145.293. View

16.

Rattani A, Wolna M, Ploquin M, Helmhart W, Morrone S, Mayer B . Sgol2 provides a regulatory platform that coordinates essential cell cycle processes during meiosis I in oocytes. Elife. 2013; 2:e01133. PMC: 3816256. DOI: 10.7554/eLife.01133. View

17.

Fu X, Cheng J, Hou Y, Zhu S . The association between the oocyte pool and aneuploidy: a comparative study of the reproductive potential of young and aged mice. J Assist Reprod Genet. 2013; 31(3):323-31. PMC: 3947073. DOI: 10.1007/s10815-013-0160-5. View

18.

MacLennan M, Crichton J, Playfoot C, Adams I . Oocyte development, meiosis and aneuploidy. Semin Cell Dev Biol. 2015; 45:68-76. PMC: 4828587. DOI: 10.1016/j.semcdb.2015.10.005. View

19.

Tang Z, Shu H, Qi W, Mahmood N, Mumby M, Yu H . PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev Cell. 2006; 10(5):575-85. DOI: 10.1016/j.devcel.2006.03.010. View

20.

Yoshizawa M, Konno H, Zhu S, Kageyama S, Fukui E, Muramatsu S . Chromosomal diagnosis in each individual blastomere of 5- to 10-cell bovine embryos derived from in vitro fertilization. Theriogenology. 2000; 51(7):1239-50. DOI: 10.1016/S0093-691X(99)00068-0. View