Impact of Global Transcriptional Silencing on Cell Cycle Regulation and Chromosome Segregation in Early Mammalian Embryos
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
17-20405 S
Grantová Agentura České Republiky
RO 0518
Ministry of Agriculture of the Czech Republic
PubMed
34445775
PubMed Central
PMC8396661
DOI
10.3390/ijms22169073
PII: ijms22169073
Knihovny.cz E-zdroje
- Klíčová slova
- cell cycle, embryo, oocyte, transcriptional repression, translation,
- MeSH
- buněčný cyklus genetika MeSH
- chromatin genetika MeSH
- embryo savčí fyziologie MeSH
- embryonální vývoj genetika MeSH
- genetická transkripce genetika MeSH
- lidé MeSH
- segregace chromozomů genetika MeSH
- umlčování genů fyziologie MeSH
- vývojová regulace genové exprese genetika MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- chromatin MeSH
The onset of an early development is, in mammals, characterized by profound changes of multiple aspects of cellular morphology and behavior. These are including, but not limited to, fertilization and the merging of parental genomes with a subsequent transition from the meiotic into the mitotic cycle, followed by global changes of chromatin epigenetic modifications, a gradual decrease in cell size and the initiation of gene expression from the newly formed embryonic genome. Some of these important, and sometimes also dramatic, changes are executed within the period during which the gene transcription is globally silenced or not progressed, and the regulation of most cellular activities, including those mentioned above, relies on controlled translation. It is known that the blastomeres within an early embryo are prone to chromosome segregation errors, which might, when affecting a significant proportion of a cell within the embryo, compromise its further development. In this review, we discuss how the absence of transcription affects the transition from the oocyte to the embryo and what impact global transcriptional silencing might have on the basic cell cycle and chromosome segregation controlling mechanisms.
Zobrazit více v PubMed
Clarke H.J. Regulation of germ cell development by intercellular signaling in the mammalian ovarian follicle. Wiley Interdiscip. Rev. Dev. Biol. 2018;7:e294. doi: 10.1002/wdev.294. PubMed DOI PMC
Kalous J., Tetkova A., Kubelka M., Susor A. Importance of ERK1/2 in Regulation of Protein Translation during Oocyte Meiosis. Int. J. Mol. Sci. 2018;19:698. doi: 10.3390/ijms19030698. PubMed DOI PMC
Jessus C., Munro C., Houliston E. Managing the Oocyte Meiotic Arrest-Lessons from Frogs and Jellyfish. Cells. 2020;9:1150. doi: 10.3390/cells9051150. PubMed DOI PMC
Bhakta H.H., Refai F.H., Avella M.A. The molecular mechanisms mediating mammalian fertilization. Development. 2019;146:dev176966. doi: 10.1242/dev.176966. PubMed DOI
Saunders C.M., Larman M.G., Parrington J., Cox L.J., Royse J., Blayney L.M., Swann K., Lai F.A. PLC zeta: A sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development. 2002;129:3533–3544. doi: 10.1242/dev.129.15.3533. PubMed DOI
Clift D., Schuh M. Restarting life: Fertilization and the transition from meiosis to mitosis. Nat. Rev. Mol. Cell Biol. 2013;14:549–562. doi: 10.1038/nrm3643. PubMed DOI PMC
Reichmann J., Nijmeijer B., Hossain M.J., Eguren M., Schneider I., Politi A.Z., Roberti M.J., Hufnagel L., Hiiragi T., Ellenberg J. Dual-spindle formation in zygotes keeps parental genomes apart in early mammalian embryos. Science. 2018;361:189–193. doi: 10.1126/science.aar7462. PubMed DOI
Cavazza T., Takeda Y., Politi A.Z., Aushev M., Aldag P., Baker C., Choudhary M., Bucevičius J., Lukinavičius G., Elder K., et al. Parental genome unification is highly error-prone in mammalian embryos. Cell. 2021;184:2860–2877.e22. doi: 10.1016/j.cell.2021.04.013. PubMed DOI PMC
Schultz R.M., Stein P., Svoboda P. The oocyte-to-embryo transition in mouse: Past, present, and future. Biol. Reprod. 2018;99:160–174. doi: 10.1093/biolre/ioy013. PubMed DOI PMC
Debey P., Szöllösi M.S., Szöllösi D., Vautier D., Girousse A., Besombes D. Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol. Reprod. Dev. 1993;36:59–74. doi: 10.1002/mrd.1080360110. PubMed DOI
Longo F., Garagna S., Merico V., Orlandini G., Gatti R., Scandroglio R., Redi C.A., Zuccotti M. Nuclear localization of NORs and centromeres in mouse oocytes during folliculogenesis. Mol. Reprod. Dev. 2003;66:279–290. doi: 10.1002/mrd.10354. PubMed DOI
Tan J.H., Wang H.L., Sun X.S., Liu Y., Sui H.S., Zhang J. Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol. Hum. Reprod. 2009;15:1–9. doi: 10.1093/molehr/gan069. PubMed DOI
Turner S., Wong H.P., Rai J., Hartshorne G.M. Telomere lengths in human oocytes, cleavage stage embryos and blastocysts. Mol. Hum. Reprod. 2010;16:685–694. doi: 10.1093/molehr/gaq048. PubMed DOI PMC
Bonnet-Garnier A., Feuerstein P., Chebrout M., Fleurot R., Jan H.U., Debey P., Beaujean N. Genome organization and epigenetic marks in mouse germinal vesicle oocytes. Int. J. Dev. Biol. 2012;56:877–887. doi: 10.1387/ijdb.120149ab. PubMed DOI
Tadros W., Lipshitz H.D. The maternal-to-zygotic transition: A play in two acts. Development. 2009;136:3033–3042. doi: 10.1242/dev.033183. PubMed DOI
Vastenhouw N.L., Cao W.X., Lipshitz H.D. The maternal-to-zygotic transition revisited. Development. 2019;146:dev161471. doi: 10.1242/dev.161471. PubMed DOI
Xue Z., Huang K., Cai C., Cai L., Jiang C.Y., Feng Y., Liu Z., Zeng Q., Cheng L., Sun Y.E., et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature. 2013;500:593–597. doi: 10.1038/nature12364. PubMed DOI PMC
Abe K.I., Funaya S., Tsukioka D., Kawamura M., Suzuki Y., Suzuki M.G., Schultz R.M., Aoki F. Minor zygotic gene activation is essential for mouse preimplantation development. Proc. Natl. Acad. Sci. USA. 2018;115:E6780–E6788. doi: 10.1073/pnas.1804309115. PubMed DOI PMC
Sha Q.Q., Zhu Y.Z., Li S., Jiang Y., Chen L., Sun X.H., Shen L., Ou X.H., Fan H.Y. Characterization of zygotic genome activation-dependent maternal mRNA clearance in mouse. Nucleic Acids Res. 2020;48:879–894. doi: 10.1093/nar/gkz1111. PubMed DOI PMC
Sha Q.Q., Zheng W., Wu Y.W., Li S., Guo L., Zhang S., Lin G., Ou X.H., Fan H.Y. Dynamics and clinical relevance of maternal mRNA clearance during the oocyte-to-embryo transition in humans. Nat. Commun. 2020;11:4917. doi: 10.1038/s41467-020-18680-6. PubMed DOI PMC
Lee M.T., Bonneau A.R., Giraldez A.J. Zygotic genome activation during the maternal-to-zygotic transition. Annu. Rev. Cell Dev. Biol. 2014;30:581–613. doi: 10.1146/annurev-cellbio-100913-013027. PubMed DOI PMC
Jukam D., Shariati S.A.M., Skotheim J.M. Zygotic Genome Activation in Vertebrates. Dev. Cell. 2017;42:316–332. doi: 10.1016/j.devcel.2017.07.026. PubMed DOI PMC
Flyamer I.M., Gassler J., Imakaev M., Brandão H.B., Ulianov S.V., Abdennur N., Razin S.V., Mirny L.A., Tachibana-Konwalski K. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature. 2017;544:110–114. doi: 10.1038/nature21711. PubMed DOI PMC
Halstead M.M., Ma X., Zhou C., Schultz R.M., Ross P.J. Chromatin remodeling in bovine embryos indicates species-specific regulation of genome activation. Nat. Commun. 2020;11:4654. doi: 10.1038/s41467-020-18508-3. PubMed DOI PMC
Hug C.B., Vaquerizas J.M. The Birth of the 3D Genome during Early Embryonic Development. Trends Genet. 2018;34:903–914. doi: 10.1016/j.tig.2018.09.002. PubMed DOI
Aoki F., Worrad D.M., Schultz R.M. Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 1997;181:296–307. doi: 10.1006/dbio.1996.8466. PubMed DOI
Latham K.E., Garrels J.I., Chang C., Solter D. Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one- and two-cell stages. Development. 1991;112:921–932. doi: 10.1242/dev.112.4.921. PubMed DOI
Hamatani T., Carter M.G., Sharov A.A., Ko M.S.H. Dynamics of Global Gene Expression Changes during Mouse Preimplantation Development. Dev. Cell. 2004;6:117–131. doi: 10.1016/S1534-5807(03)00373-3. PubMed DOI
Vassena R., Boué S., González-Roca E., Aran B., Auer H., Veiga A., Izpisua Belmonte J.C. Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development. 2011;138:3699–3709. doi: 10.1242/dev.064741. PubMed DOI PMC
Memili E., First N.L. Zygotic and embryonic gene expression in cow: A review of timing and mechanisms of early gene expression as compared with other species. Zygote. 2000;8:87–96. doi: 10.1017/S0967199400000861. PubMed DOI
Misirlioglu M., Page G.P., Sagirkaya H., Kaya A., Parrish J.J., First N.L., Memili E. Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc. Natl. Acad. Sci. USA. 2006;103:18905–18910. doi: 10.1073/pnas.0608247103. PubMed DOI PMC
Graf A., Krebs S., Zakhartchenko V., Schwalb B., Blum H., Wolf E. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc. Natl. Acad. Sci. USA. 2014;111:4139–4144. doi: 10.1073/pnas.1321569111. PubMed DOI PMC
Abe K., Yamamoto R., Franke V., Cao M., Suzuki Y., Suzuki M.G., Vlahovicek K., Svoboda P., Schultz R.M., Aoki F. The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3’ processing. EMBO J. 2015;34:1523–1537. doi: 10.15252/embj.201490648. PubMed DOI PMC
Hochegger H., Takeda S., Hunt T. Cyclin-dependent kinases and cell-cycle transitions: Does one fit all. Nat. Rev. Mol. Cell Biol. 2008;9:910–916. doi: 10.1038/nrm2510. PubMed DOI
Koliopoulos M.G., Alfieri C. Cell cycle regulation by complex nanomachines. FEBS J. 2021 doi: 10.1111/febs.16082. PubMed DOI
Gelens L., Qian J., Bollen M., Saurin A.T. The Importance of Kinase-Phosphatase Integration: Lessons from Mitosis. Trends Cell Biol. 2018;28:6–21. doi: 10.1016/j.tcb.2017.09.005. PubMed DOI
Holder J., Poser E., Barr F.A. Getting out of mitosis: Spatial and temporal control of mitotic exit and cytokinesis by PP1 and PP2A. FEBS Lett. 2019;593:2908–2924. doi: 10.1002/1873-3468.13595. PubMed DOI
Peters J.M. The anaphase-promoting complex: Proteolysis in mitosis and beyond. Mol. Cell. 2002;9:931–943. doi: 10.1016/S1097-2765(02)00540-3. PubMed DOI
Acquaviva C., Pines J. The anaphase-promoting complex/cyclosome: APC/C. J. Cell Sci. 2006;119:2401–2404. doi: 10.1242/jcs.02937. PubMed DOI
Cogswell J.P., Godlevski M.M., Bonham M., Bisi J., Babiss L. Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter. Mol. Cell Biol. 1995;15:2782–2790. doi: 10.1128/MCB.15.5.2782. PubMed DOI PMC
King R.W., Peters J.M., Tugendreich S., Rolfe M., Hieter P., Kirschner M.W. A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell. 1995;81:279–288. doi: 10.1016/0092-8674(95)90338-0. PubMed DOI
Brandeis M., Hunt T. The proteolysis of mitotic cyclins in mammalian cells persists from the end of mitosis until the onset of S phase. EMBO J. 1996;15:5280–5289. doi: 10.1002/j.1460-2075.1996.tb00913.x. PubMed DOI PMC
Wasner M., Tschöp K., Spiesbach K., Haugwitz U., Johne C., Mössner J., Mantovani R., Engeland K. Cyclin B1 transcription is enhanced by the p300 coactivator and regulated during the cell cycle by a CHR-dependent repression mechanism. FEBS Lett. 2003;536:66–70. doi: 10.1016/S0014-5793(03)00028-0. PubMed DOI
Palozola K.C., Lerner J., Zaret K.S. A changing paradigm of transcriptional memory propagation through mitosis. Nat. Rev. Mol. Cell Biol. 2019;20:55–64. doi: 10.1038/s41580-018-0077-z. PubMed DOI PMC
Palozola K.C., Donahue G., Liu H., Grant G.R., Becker J.S., Cote A., Yu H., Raj A., Zaret K.S. Mitotic transcription and waves of gene reactivation during mitotic exit. Science. 2017;358:119–122. doi: 10.1126/science.aal4671. PubMed DOI PMC
Susor A., Jansova D., Anger M., Kubelka M. Translation in the mammalian oocyte in space and time. Cell Tissue Res. 2016;363:69–84. doi: 10.1007/s00441-015-2269-6. PubMed DOI
Sirard M.A., Florman H.M., Leibfried-Rutledge M.L., Barnes F.L., Sims M.L., First N.L. Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 1989;40:1257–1263. doi: 10.1095/biolreprod40.6.1257. PubMed DOI
Balakier H., MacLusky N.J., Casper R.F. Characterization of the first cell cycle in human zygotes: Implications for cryopreservation. Fertil. Steril. 1993;59:359–365. doi: 10.1016/S0015-0282(16)55678-7. PubMed DOI
Holm P., Shukri N.N., Vajta G., Booth P., Bendixen C., Callesen H. Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. Theriogenology. 1998;50:1285–1299. doi: 10.1016/S0093-691X(98)00227-1. PubMed DOI
Fancsovits P., Toth L., Takacs Z.F., Murber A., Papp Z., Urbancsek J. Early pronuclear breakdown is a good indicator of embryo quality and viability. Fertil. Steril. 2005;84:881–887. doi: 10.1016/j.fertnstert.2005.03.068. PubMed DOI
Jones K.T. Mammalian egg activation: From Ca2+ spiking to cell cycle progression. Reproduction. 2005;130:813–823. doi: 10.1530/rep.1.00710. PubMed DOI
Radonova L., Svobodova T., Anger M. Regulation of the cell cycle in early mammalian embryos and its clinical implications. Int. J. Dev. Biol. 2019;63:113–122. doi: 10.1387/ijdb.180400ma. PubMed DOI
Chao H.X., Fakhreddin R.I., Shimerov H.K., Kedziora K.M., Kumar R.J., Perez J., Limas J.C., Grant G.D., Cook J.G., Gupta G.P., et al. Evidence that the human cell cycle is a series of uncoupled, memoryless phases. Mol. Syst. Biol. 2019;15:e8604. doi: 10.15252/msb.20188604. PubMed DOI PMC
Ciemerych M.A., Sicinski P. Cell cycle in mouse development. Oncogene. 2005;24:2877–2898. doi: 10.1038/sj.onc.1208608. PubMed DOI
Satyanarayana A., Kaldis P. Mammalian cell-cycle regulation: Several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene. 2009;28:2925–2939. doi: 10.1038/onc.2009.170. PubMed DOI
Palmer N., Kaldis P. Regulation of the Embryonic Cell Cycle During Mammalian Preimplantation Development. Curr. Top. Dev. Biol. 2016;120:1–53. PubMed
Chotiner J.Y., Wolgemuth D.J., Wang P.J. Functions of cyclins and CDKs in mammalian gametogenesis†. Biol. Reprod. 2019;101:591–601. doi: 10.1093/biolre/ioz070. PubMed DOI PMC
Campbell G.J., Hands E.L., Van de Pette M. The Role of CDKs and CDKIs in Murine Development. Int. J. Mol. Sci. 2020;21:6343. doi: 10.3390/ijms21155343. PubMed DOI PMC
Kozar K., Ciemerych M.A., Rebel V.I., Shigematsu H., Zagozdzon A., Sicinska E., Geng Y., Yu Q., Bhattacharya S., Bronson R.T., et al. Mouse development and cell proliferation in the absence of D-cyclins. Cell. 2004;118:477–491. doi: 10.1016/j.cell.2004.07.025. PubMed DOI
Geng Y., Yu Q., Sicinska E., Das M., Schneider J.E., Bhattacharya S., Rideout W.M., Bronson R.T., Gardner H., Sicinski P. Cyclin E Ablation in the Mouse. Cell. 2003;114:431–443. doi: 10.1016/S0092-8674(03)00645-7. PubMed DOI
Parisi T., Beck A.R., Rougier N., McNeil T., Lucian L., Werb Z., Amati B. Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. EMBO J. 2003;22:4794–4803. doi: 10.1093/emboj/cdg482. PubMed DOI PMC
Brandeis M., Rosewell I., Carrington M., Crompton T., Jacobs M.A., Kirk J., Gannon J., Hunt T. Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc. Natl. Acad. Sci. USA. 1998;95:4344–4349. doi: 10.1073/pnas.95.8.4344. PubMed DOI PMC
Strauss B., Harrison A., Coelho P.A., Yata K., Zernicka-Goetz M., Pines J. Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis. J. Cell Biol. 2018;217:179–193. doi: 10.1083/jcb.201612147. PubMed DOI PMC
Zhang Q.H., Yuen W.S., Adhikari D., Flegg J.A., FitzHarris G., Conti M., Sicinski P., Nabti I., Marangos P., Carroll J. Cyclin A2 modulates kinetochore-microtubule attachment in meiosis II. J. Cell Biol. 2017;216:3133–3143. doi: 10.1083/jcb.201607111. PubMed DOI PMC
Murphy M. Delayed early embryonic lethality following disruption of the murine cyclin A2 gene. Nat. Genet. 1999;23:481. doi: 10.1038/70612. PubMed DOI
Hara K.T., Oda S., Naito K., Nagata M., Schultz R.M., Aoki F. Cyclin A2-CDK2 regulates embryonic gene activation in 1-cell mouse embryos. Dev. Biol. 2005;286:102–113. doi: 10.1016/j.ydbio.2005.07.012. PubMed DOI
Pagliuca F.W., Collins M.O., Lichawska A., Zegerman P., Choudhary J.S., Pines J. Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol. Cell. 2011;43:406–417. doi: 10.1016/j.molcel.2011.05.031. PubMed DOI PMC
Hégarat N., Crncec A., Suarez Peredo Rodriguez M.F., Echegaray Iturra F., Gu Y., Busby O., Lang P.F., Barr A.R., Bakal C., Kanemaki M.T., et al. Cyclin A triggers Mitosis either via the Greatwall kinase pathway or Cyclin B. EMBO J. 2020;39:e104419. doi: 10.15252/embj.2020104419. PubMed DOI PMC
Kanakkanthara A., Jeganathan K.B., Limzerwala J.F., Baker D.J., Hamada M., Nam H.J., van Deursen W.H., Hamada N., Naylor R.M., Becker N.A., et al. Cyclin A2 is an RNA binding protein that controls Mre11 mRNA translation. Science. 2016;353:1549–1552. doi: 10.1126/science.aaf7463. PubMed DOI PMC
Kalaszczynska I., Geng Y., Iino T., Mizuno S., Choi Y., Kondratiuk I., Silver D.P., Wolgemuth D.J., Akashi K., Sicinski P. Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells. Cell. 2009;138:352–365. doi: 10.1016/j.cell.2009.04.062. PubMed DOI PMC
Santamaría D., Barrière C., Cerqueira A., Hunt S., Tardy C., Newton K., Cáceres J.F., Dubus P., Malumbres M., Barbacid M. Cdk1 is sufficient to drive the mammalian cell cycle. Nature. 2007;448:811–815. doi: 10.1038/nature06046. PubMed DOI
Diril M.K., Ratnacaram C.K., Padmakumar V.C., Du T., Wasser M., Coppola V., Tessarollo L., Kaldis P. Cyclin-dependent kinase 1 (Cdk1) is essential for cell division and suppression of DNA re-replication but not for liver regeneration. Proc. Natl. Acad. Sci. USA. 2012;109:3826–3831. doi: 10.1073/pnas.1115201109. PubMed DOI PMC
Pagano M., Jackson P.K. Wagging the dogma; tissue-specific cell cycle control in the mouse embryo. Cell. 2004;118:535–538. doi: 10.1016/j.cell.2004.08.013. PubMed DOI
Susor A., Kubelka M. Translational Regulation in the Mammalian Oocyte. Results Probl. Cell Differ. 2017;63:257–295. PubMed
Sha Q.Q., Zhang J., Fan H.Y. A story of birth and death: mRNA translation and clearance at the onset of Maternal-to-Zygotic transition in mammals. Biol. Reprod. 2019;101:579–590. doi: 10.1093/biolre/ioz012. PubMed DOI
Esencan E., Kallen A., Zhang M., Seli E. Translational activation of maternally derived mRNAs in oocytes and early embryos and the role of embryonic poly(A) binding protein (EPAB) Biol. Reprod. 2019;100:1147–1157. doi: 10.1093/biolre/ioz034. PubMed DOI PMC
Gonzalez L., Nebreda A.R. RINGO/Speedy proteins, a family of non-canonical activators of CDK1 and CDK2. Semin. Cell Dev. Biol. 2020;107:21–27. doi: 10.1016/j.semcdb.2020.03.010. PubMed DOI
Vassalli J.D., Huarte J., Belin D., Gubler P., Vassalli A., O’Connell M.L., Parton L.A., Rickles R.J., Strickland S. Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 1989;3:2163–2171. doi: 10.1101/gad.3.12b.2163. PubMed DOI
McGrew L.L., Dworkin-Rastl E., Dworkin M.B., Richter J.D. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 1989;3:803–815. doi: 10.1101/gad.3.6.803. PubMed DOI
Groisman I., Jung M.Y., Sarkissian M., Cao Q., Richter J.D. Translational control of the embryonic cell cycle. Cell. 2002;109:473–483. doi: 10.1016/S0092-8674(02)00733-X. PubMed DOI
Richter J.D. CPEB: A life in translation. Trends Biochem. Sci. 2007;32:279–285. doi: 10.1016/j.tibs.2007.04.004. PubMed DOI
Seli E., Lalioti M.D., Flaherty S.M., Sakkas D., Terzi N., Steitz J.A. An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos. Proc. Natl. Acad. Sci. USA. 2005;102:367–372. doi: 10.1073/pnas.0408378102. PubMed DOI PMC
Kronja I., Orr-Weaver T.L. Translational regulation of the cell cycle: When, where, how and why. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2011;366:3638–3652. doi: 10.1098/rstb.2011.0084. PubMed DOI PMC
Yang Y., Yang C.R., Han S.J., Daldello E.M., Cho A., Martins J.P.S., Xia G., Conti M. Maternal mRNAs with distinct 3’ UTRs define the temporal pattern of Ccnb1 synthesis during mouse oocyte meiotic maturation. Genes Dev. 2017;31:1302–1307. doi: 10.1101/gad.296871.117. PubMed DOI PMC
Yatskevich S., Rhodes J., Nasmyth K. Organization of Chromosomal DNA by SMC Complexes. Annu. Rev. Genet. 2019;53:445–482. doi: 10.1146/annurev-genet-112618-043633. PubMed DOI
Waizenegger I.C., Hauf S., Meinke A., Peters J.M. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell. 2000;103:399–410. doi: 10.1016/S0092-8674(00)00132-X. PubMed DOI
Perea-Resa C., Bury L., Cheeseman I.M., Blower M.D. Cohesin Removal Reprograms Gene Expression upon Mitotic Entry. Mol. Cell. 2020;78:127–140.e7. doi: 10.1016/j.molcel.2020.01.023. PubMed DOI PMC
Ciosk R., Zachariae W., Michaelis C., Shevchenko A., Mann M., Nasmyth K. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell. 1998;93:1067–1076. doi: 10.1016/S0092-8674(00)81211-8. PubMed DOI
Kamenz J., Hauf S. Time To Split Up: Dynamics of Chromosome Separation. Trends Cell Biol. 2017;27:42–54. doi: 10.1016/j.tcb.2016.07.008. PubMed DOI
Kudo N.R., Wassmann K., Anger M., Schuh M., Wirth K.G., Xu H., Helmhart W., Kudo H., McKay M., Maro B., et al. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell. 2006;126:135–146. doi: 10.1016/j.cell.2006.05.033. PubMed DOI
Tsou M.F., Stearns T. Mechanism limiting centrosome duplication to once per cell cycle. Nature. 2006;442:947–951. doi: 10.1038/nature04985. PubMed DOI
Kumar R. Separase: Function Beyond Cohesion Cleavage and an Emerging Oncogene. J. Cell Biochem. 2017;118:1283–1299. doi: 10.1002/jcb.25835. PubMed DOI
Maier N.K., Ma J., Lampson M.A., Cheeseman I.M. Separase cleaves the kinetochore protein Meikin at the meiosis I/II transition. Dev. Cell. 2021;56:2192–2206.e8. doi: 10.1016/j.devcel.2021.06.019. PubMed DOI PMC
Vijayakumari D., Müller J., Hauf S. Cdc48 influence on separase levels is independent of mitosis and suggests translational sensitivity of separase. bioRxiv. 2021 doi: 10.1101/2021.04.28.441771. PubMed DOI PMC
Meadows J.C., Millar J.B. Sharpening the anaphase switch. Biochem. Soc. Trans. 2015;43:19–22. doi: 10.1042/BST20140250. PubMed DOI
Hellmuth S., Gómez-H L., Pendás A.M., Stemmann O. Securin-independent regulation of separase by checkpoint-induced shugoshin-MAD2. Nature. 2020;580:536–541. doi: 10.1038/s41586-020-2182-3. PubMed DOI
Huang X., Andreu-Vieyra C.V., Wang M., Cooney A.J., Matzuk M.M., Zhang P. Preimplantation mouse embryos depend on inhibitory phosphorylation of separase to prevent chromosome missegregation. Mol. Cell Biol. 2009;29:1498–1505. doi: 10.1128/MCB.01778-08. PubMed DOI PMC
Li M., York J.P., Zhang P. Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. Mol. Cell Biol. 2007;27:3481–3488. doi: 10.1128/MCB.02088-06. PubMed DOI PMC
Musacchio A. The Molecular Biology of Spindle Assembly Checkpoint Signaling Dynamics. Curr. Biol. 2015;25:R1002–R1018. doi: 10.1016/j.cub.2015.08.051. PubMed DOI
Pesenti M.E., Weir J.R., Musacchio A. Progress in the structural and functional characterization of kinetochores. Curr. Opin. Struct. Biol. 2016;37:152–163. doi: 10.1016/j.sbi.2016.03.003. PubMed DOI
Nagaoka S.I., Hodges C.A., Albertini D.F., Hunt P.A. Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr. Biol. 2011;21:651–657. doi: 10.1016/j.cub.2011.03.003. PubMed DOI PMC
Sebestova J., Danylevska A., Novakova L., Kubelka M., Anger M. Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle. 2012;11:3011–3018. doi: 10.4161/cc.21398. PubMed DOI PMC
Lane S.I., Yun Y., Jones K.T. Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development. 2012;139:1947–1955. doi: 10.1242/dev.077040. PubMed DOI
Kyogoku H., Kitajima T.S. Large Cytoplasm Is Linked to the Error-Prone Nature of Oocytes. Dev. Cell. 2017;41:287–298.e4. doi: 10.1016/j.devcel.2017.04.009. PubMed DOI
Lane S.I.R., Jones K.T. Chromosome biorientation and APC activity remain uncoupled in oocytes with reduced volume. J. Cell Biol. 2017;216:3949–3957. doi: 10.1083/jcb.201606134. PubMed DOI PMC
Vázquez-Diez C., Paim L.M.G., FitzHarris G. Cell-Size-Independent Spindle Checkpoint Failure Underlies Chromosome Segregation Error in Mouse Embryos. Curr. Biol. 2019;29:865–873. doi: 10.1016/j.cub.2018.12.042. PubMed DOI
Bolton H., Graham S.J., Van der Aa N., Kumar P., Theunis K., Fernandez Gallardo E., Voet T., Zernicka-Goetz M. Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential. Nat. Commun. 2016;7:11165. doi: 10.1038/ncomms11165. PubMed DOI PMC
Pauerova T., Radonova L., Kovacovicova K., Novakova L., Skultety M., Anger M. Aneuploidy during the onset of mouse embryo development. Reproduction. 2020;160:773–782. doi: 10.1530/REP-20-0086. PubMed DOI
Tsurumi C., Hoffmann S., Geley S., Graeser R., Polanski Z. The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J. Cell Biol. 2004;167:1037–1050. doi: 10.1083/jcb.200405165. PubMed DOI PMC
Kouznetsova A., Kitajima T.S., Brismar H., Höög C. Post-metaphase correction of aberrant kinetochore-microtubule attachments in mammalian eggs. EMBO Rep. 2019;20:e47905. doi: 10.15252/embr.201947905. PubMed DOI PMC
Yun Y., Lane S.I., Jones K.T. Premature dyad separation in meiosis II is the major segregation error with maternal age in mouse oocytes. Development. 2014;141:199–208. doi: 10.1242/dev.100206. PubMed DOI PMC
Dobles M., Liberal V., Scott M.L., Benezra R., Sorger P.K. Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell. 2000;101:635–645. doi: 10.1016/S0092-8674(00)80875-2. PubMed DOI
Tian Q., Hanlon Newell A.E., Wang Y., Olson S.B., Fedorov L.M. Complex cytogenetic analysis of early lethality mouse embryos. Chromosome Res. 2011;19:567–574. doi: 10.1007/s10577-011-9209-4. PubMed DOI
Kalitsis P., Earle E., Fowler K.J., Choo K.H. Bub3 gene disruption in mice reveals essential mitotic spindle checkpoint function during early embryogenesis. Genes Dev. 2000;14:2277–2282. doi: 10.1101/gad.827500. PubMed DOI PMC
Iwanaga Y., Chi Y.H., Miyazato A., Sheleg S., Haller K., Peloponese J.M., Li Y., Ward J.M., Benezra R., Jeang K.T. Heterozygous deletion of mitotic arrest-deficient protein 1 (MAD1) increases the incidence of tumors in mice. Cancer Res. 2007;67:160–166. doi: 10.1158/0008-5472.CAN-06-3326. PubMed DOI
Wang Q., Liu T., Fang Y., Xie S., Huang X., Mahmood R., Ramaswamy G., Sakamoto K.M., Darzynkiewicz Z., Xu M., et al. BUBR1 deficiency results in abnormal megakaryopoiesis. Blood. 2004;103:1278–1285. doi: 10.1182/blood-2003-06-2158. PubMed DOI
Jeganathan K., Malureanu L., Baker D.J., Abraham S.C., van Deursen J.M. Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J. Cell Biol. 2007;179:255–267. doi: 10.1083/jcb.200706015. PubMed DOI PMC
Wells D., Bermudez M.G., Steuerwald N., Thornhill A.R., Walker D.L., Malter H., Delhanty J.D., Cohen J. Expression of genes regulating chromosome segregation, the cell cycle and apoptosis during human preimplantation development. Hum. Reprod. 2005;20:1339–1348. doi: 10.1093/humrep/deh778. PubMed DOI
Eliscovich C., Peset I., Vernos I., Méndez R. Spindle-localized CPE-mediated translation controls meiotic chromosome segregation. Nat. Cell Biol. 2008;10:858–865. doi: 10.1038/ncb1746. PubMed DOI
Hassold T., Hunt P. To err (meiotically) is human: The genesis of human aneuploidy. Nat. Rev. Genet. 2001;2:280–291. doi: 10.1038/35066065. PubMed DOI
Nagaoka S.I., Hassold T.J., Hunt P.A. Human aneuploidy: Mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 2012;13:493–504. doi: 10.1038/nrg3245. PubMed DOI PMC
Van Echten-Arends J., Mastenbroek S., Sikkema-Raddatz B., Korevaar J.C., Heineman M.J., van der Veen F., Repping S. Chromosomal mosaicism in human preimplantation embryos: A systematic review. Hum. Reprod. Update. 2011;17:620–627. doi: 10.1093/humupd/dmr014. PubMed DOI
Ben-David U., Amon A. Context is everything: Aneuploidy in cancer. Nat. Rev. Genet. 2020;21:44–62. doi: 10.1038/s41576-019-0171-x. PubMed DOI
Chromosome Division in Early Embryos-Is Everything under Control? And Is the Cell Size Important?