FBXO34 Regulates the G2/M Transition and Anaphase Entry in Meiotic Oocytes

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2021 Apr 12

PMID 33842473

Citations 7

Authors

Bing-Wang Zhao

Si-Min Sun

Ke Xu

Yuan-Yuan Li

Wen-Long Lei

Li Li

Sai-Li Liu

Ying-Chun Ouyang

Qing-Yuan Sun

Zhen-Bo Wang

Affiliations

Soon will be listed here.

Abstract

There are two important events in oocyte meiotic maturation, the G2/M transition and metaphase I progression. Thousands of proteins participate in regulating oocyte maturation, which highlights the importance of the ubiquitin proteasome system (UPS) in regulating protein synthesis and degradation. Skp1-Cullin-F-box (SCF) complexes, as the best characterized ubiquitin E3 ligases in the UPS, specifically recognize their substrates. F-box proteins, as the variable adaptors of SCF, can bind substrates specifically. Little is known about the functions of the F-box proteins in oocyte maturation. In this study, we found that depletion of FBXO34, an F-box protein, led to failure of oocyte meiotic resumption due to a low activity of MPF, and this phenotype could be rescued by exogenous overexpression of CCNB1. Strikingly, overexpression of FBXO34 promoted germinal vesicle breakdown (GVBD), but caused continuous activation of spindle assembly checkpoint (SAC) and MI arrest of oocytes. Here, we demonstrated that FBXO34 regulated both the G2/M transition and anaphase entry in meiotic oocytes.

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References

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

Gopinathan L, Szmyd R, Low D, Diril M, Chang H, Coppola V . Emi2 Is Essential for Mouse Spermatogenesis. Cell Rep. 2017; 20(3):697-708. PMC: 7974383. DOI: 10.1016/j.celrep.2017.06.033. View

Marangos P, Verschuren E, Chen R, Jackson P, Carroll J . Prophase I arrest and progression to metaphase I in mouse oocytes are controlled by Emi1-dependent regulation of APC(Cdh1). J Cell Biol. 2006; 176(1):65-75. PMC: 2063628. DOI: 10.1083/jcb.200607070. View

Stitzel M, Seydoux G . Regulation of the oocyte-to-zygote transition. Science. 2007; 316(5823):407-8. DOI: 10.1126/science.1138236. View

Kisielnicka E, Minasaki R, Eckmann C . MAPK signaling couples SCF-mediated degradation of translational regulators to oocyte meiotic progression. Proc Natl Acad Sci U S A. 2018; 115(12):E2772-E2781. PMC: 5866554. DOI: 10.1073/pnas.1715439115. View

Li J, Dong F, Ouyang Y, Sun Q, Qian W . Overexpression of cyclin A1 promotes meiotic resumption but induces premature chromosome separation in mouse oocyte. J Cell Physiol. 2020; 235(10):7136-7145. DOI: 10.1002/jcp.29612. View

Mitra J, Schultz R . Regulation of the acquisition of meiotic competence in the mouse: changes in the subcellular localization of cdc2, cyclin B1, cdc25C and wee1, and in the concentration of these proteins and their transcripts. J Cell Sci. 1996; 109 ( Pt 9):2407-15. DOI: 10.1242/jcs.109.9.2407. View

Stegmeier F, Rape M, Draviam V, Nalepa G, Sowa M, Ang X . Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature. 2007; 446(7138):876-81. DOI: 10.1038/nature05694. View

Jin Y, Yang M, Gao C, Yue W, Liang X, Xie B . Fbxo30 regulates chromosome segregation of oocyte meiosis. Cell Mol Life Sci. 2019; 76(11):2217-2229. PMC: 11105211. DOI: 10.1007/s00018-019-03038-z. View

10.

Dumont J, Desai A . Acentrosomal spindle assembly and chromosome segregation during oocyte meiosis. Trends Cell Biol. 2012; 22(5):241-9. PMC: 3348331. DOI: 10.1016/j.tcb.2012.02.007. View

11.

Cepeda D, Ng H, Sharifi H, Mahmoudi S, Cerrato V, Fredlund E . CDK-mediated activation of the SCF(FBXO) (28) ubiquitin ligase promotes MYC-driven transcription and tumourigenesis and predicts poor survival in breast cancer. EMBO Mol Med. 2013; 5(7):1067-86. PMC: 3721474. DOI: 10.1002/emmm.201202341. View

12.

Zhang P, Ni X, Guo Y, Guo X, Wang Y, Zhou Z . Proteomic-based identification of maternal proteins in mature mouse oocytes. BMC Genomics. 2009; 10:348. PMC: 2730056. DOI: 10.1186/1471-2164-10-348. View

13.

Ciechanover A . The ubiquitin-proteasome proteolytic pathway. Cell. 1994; 79(1):13-21. DOI: 10.1016/0092-8674(94)90396-4. View

14.

Cardozo T, Pagano M . The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol. 2004; 5(9):739-51. DOI: 10.1038/nrm1471. View

15.

Reddy S, Rape M, Margansky W, Kirschner M . Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature. 2007; 446(7138):921-5. DOI: 10.1038/nature05734. View

16.

Li M, Li S, Yuan J, Wang Z, Sun S, Schatten H . Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. PLoS One. 2009; 4(11):e7701. PMC: 2765619. DOI: 10.1371/journal.pone.0007701. View

17.

Kipreos E, Pagano M . The F-box protein family. Genome Biol. 2001; 1(5):REVIEWS3002. PMC: 138887. DOI: 10.1186/gb-2000-1-5-reviews3002. View

18.

Matzuk M, Burns K, Viveiros M, Eppig J . Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002; 296(5576):2178-80. DOI: 10.1126/science.1071965. View

19.

Pickart C . Back to the future with ubiquitin. Cell. 2004; 116(2):181-90. DOI: 10.1016/s0092-8674(03)01074-2. View

20.

Kinterova V, Kanka J, Petruskova V, Toralova T . Inhibition of Skp1-Cullin-F-box complexes during bovine oocyte maturation and preimplantation development leads to delayed development of embryos†. Biol Reprod. 2018; 100(4):896-906. DOI: 10.1093/biolre/ioy254. View