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Review

Cycling through mammalian meiosis: B-type cyclins in oocytes

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Pages 1537-1548 | Received 03 May 2019, Accepted 24 May 2019, Published online: 23 Jun 2019

References

  • El Yakoubi W, Wassmann K. Meiotic divisions: no place for gender equality. In: Gotta M, Meraldi P, editors. Cell division machinery and disease. Cham: Springer International Publishing; 2017. p. 1–17. Advances in Experimental Medicine and Biology. DOI:10.1007/978-3-319-57127-0_1
  • Holt JE, Lane SIR, Jones KT. Chapter seven - The control of meiotic maturation in mammalian oocytes. In: Wassarman PM, editor. Current topics in developmental biology. Vol. 102. Gametogenesis: Academic Press; 2013. p. 207–226.
  • Herbert M, Kalleas D, Cooney D, et al. Meiosis and maternal aging: insights from aneuploid oocytes and trisomy births. Cold Spring Harb Perspect Biol. 2015;7(4):a017970.
  • Templado C, Uroz L, Estop A. New insights on the origin and relevance of aneuploidy in human spermatozoa. Mol Hum Reprod. 2013;19(10):634–643.
  • Hassold T, Hunt P. To Err (Meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet. 2001;2(4):280.
  • Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet. 2012;13(7):493–504.
  • Touati SA, Wassmann K. How oocytes try to get it right: spindle checkpoint control in meiosis. Chromosoma. 2016;125(2):321–335.
  • Capalbo A, Hoffmann ER, Cimadomo D, et al. Human female meiosis revised: new insights into the mechanisms of chromosome segregation and aneuploidies from advanced genomics and time-lapse imaging. Hum Reprod Update. 2017;23(6):706–722.
  • Vázquez-Diez C, FitzHarris G. Causes and consequences of chromosome segregation error in preimplantation embryos. Reproduction. 2018;155(1):R63–76.
  • Schneider I, Ellenberg J. Mysteries in embryonic development: how can errors arise so frequently at the beginning of mammalian life? PLoS Biol. 2019;17(3):e3000173.
  • Sanders JR, Jones KT. Regulation of the meiotic divisions of mammalian oocytes and eggs. Biochem Soc Trans. 2018;46(4):797–806.
  • Wassmann K. Sister chromatid segregation in meiosis II : deprotection through phosphorylation. Cell Cycle. 2013;12(9):1352–1359.
  • Pines J, Hunter T. Isolation of a human cyclin CDNA: evidence for cyclin MRNA and protein regulation in the cell cycle and for interaction with P34cdc2. Cell. 1989;58(5):833–846.
  • Chapman DL, Wolgemuth DJ. Identification of a Mouse B-type cyclin which exhibits developmentally regulated expression in the germ line. Mol Reprod Dev. 1992;33(3):259–269.
  • Nieduszynski CA, Murray J, Carrington M. Whole-genome analysis of animal A- and B-type cyclins. Genome Biol. 2002;3(12). research0070.1. DOI:10.1186/gb-2002-3-12-research0070
  • Jian L, Tang J-X, Cheng J-M, et al. Cyclin B2 can compensate for cyclin B1 in oocyte meiosis I. J Cell Biol. 2018;217(11):3901–3911.
  • Karasu ME, Keeney S. Cyclin B3 is dispensable for mouse spermatogenesis. BioRxiv. 2019 April;608315. DOI:10.1101/608315
  • Karasu ME, Bouftas N, Keeney S, et al. Cyclin B3 promotes anaphase I onset in oocyte meiosis. J Cell Biol. 2019 February:201808091. jcb. DOI:10.1083/jcb.201808091
  • Yufei L, Wang L, Zhang L, et al. Cyclin B3 is required for metaphase to anaphase transition in oocyte meiosis I. J Cell Biol. 2019 February:201808088. jcb. DOI:10.1083/jcb.201808088
  • Brandeis M, Rosewell I, Carrington M, et al. Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc Nat Acad Sci. 1998;95(8):4344–4349.
  • Daldello EM, Luong XG, Yang C-R, et al. Cyclin B2 is required for progression through meiosis in mouse oocytes. Development. 2019;146:172734. April, dev.
  • Gorbsky GJ. The spindle checkpoint and chromosome segregation in meiosis. Febs J. 2015;282(13):2458–2474.
  • Homer H. The APC/C in female mammalian meiosis I. Reproduction. 2013;146(2):R61–71.
  • Emilie TM, Wassmann K, Waizenegger I, et al. The Meiosis I-to-Meiosis II transition in mouse oocytes requires separase activity. Curr Biol. 2003;13(20):1797–1802.
  • Herbert M, Levasseur M, Homer H, et al. Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat Cell Biol. 2003;5(11):1023–1025.
  • Kudo NR, Wassmann K, Anger M, et al. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell. 2006;126:135–146.
  • Runft LL, Jaffe LA, Mehlmann LM. Egg activation at fertilization: where it all begins. Dev Biol. 2002;245(2):237–254.
  • Perry ACF, Verlhac M-H. Second meiotic arrest and exit in frogs and mice. EMBO Rep. 2008;9(3):246–251.
  • Kishimoto T. Entry into mitosis: a solution to the decades-long enigma of MPF. Chromosoma. 2015;124(4):417–428.
  • Vigneron S, Robert P, Hached K, et al. The master greatwall kinase, a critical regulator of mitosis and meiosis. Int J Dev Biol. 2016;60(7–8–9):245–254.
  • Adhikari D, Liu K. The regulation of maturation promoting factor during Prophase I arrest and meiotic entry in mammalian oocytes. Mol Cell Endocrinol. 2014;382(1):480–487.
  • Han SJ, Conti M. New pathways from PKA to the Cdc2/Cyclin B complex in oocytes: wee1B as a potential PKA substrate. Cell Cycle. 2006;5(3):227–231.
  • Solc P, Schultz RM, Motlik J. Prophase I arrest and progression to metaphase I in mouse oocytes: comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Mol Hum Reprod. 2010;16(9):654–664.
  • Richardson H, Lew DJ, Henze M, et al. Cyclin-B homologs in saccharomyces cerevisiae function in S phase and in G2. Genes Dev. 1992;6(11):2021–2034.
  • Gutiérrez-Escribano P, Nurse P. A single cyclin–CDK complex is sufficient for both mitotic and meiotic progression in fission yeast. Nat Commun. 2015;6(1):6871.
  • Fisher DL, Nurse P. A single fission yeast mitotic cyclin B P34cdc2 kinase promotes both S-phase and mitosis in the absence of G1 cyclins. Embo J. 1996;15(4):850–860.
  • McGuinness BE, Anger M, Anna Kouznetsova AM, et al. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol. 2009;19(5):369–380.
  • Wassmann K, Niault T, Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol. 2003;13(18):1596–1608.
  • Ledan E, Polanski Z, Terret M-E, et al. Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Dev Biol. 2001;232(2):400–413.
  • Reis A, Madgwick S, Chang H-Y, et al. Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nat Cell Biol. 2007;9(10):1192–1198.
  • Jones KT. Mammalian egg activation: from Ca2+ spiking to cell cycle progression. Reproduction. 2005;130(6):813–823.
  • Vantéry C, de Gavin AC, Vassalli JD, et al. An accumulation of P34cdc2at the end of mouse oocyte growth correlates with the acquisition of meiotic competence. Dev Biol. 1996;174(2):335–344.
  • Hashimoto N, Kishimoto T. Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev Biol. 1988;126(2):242–252.
  • Levasseur MD, Thomas C, Davies OR, et al. Aneuploidy in oocytes is prevented by sustained CDK1 activity through degron masking in cyclin B1. Dev Cell. 2019February;48:672–684.e5.
  • Arooz T, Yam CH, Siu WY, et al. On the concentrations of cyclins and cyclin-dependent kinases in extracts of cultured human cells. Biochemistry. 2000;39(31):9494–9501.
  • Hellmuth S, Böttger F, Pan C, et al. PP2A delays APC/C‐dependent degradation of separase‐associated but not free securin. Embo J. 2014;33(10):1134–1147.
  • Holt LJ, Krutchinsky AN, Morgan DO. Positive feedback sharpens the anaphase switch. Nature. 2008;454(7202):353–357.
  • Touati SA, Cladière D, Lister LM, et al. Cyclin A2 is required for sister chromatid segregation, but not separase control, in mouse oocyte meiosis. Cell Rep. 2012;2(5):1077–1087.
  • Konishi M, Shindo N, Komiya M, et al. Quantitative analyses of the metaphase-to-anaphase transition reveal differential kinetic regulation for securin and cyclin B1. Biomed Res. 2018;39(2):75–85.
  • Kubiak JZ, Weber M, de Pennart H, et al. The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. Embo J. 1993;12(10):3773–3778.
  • Nixon VL, Levasseur M, McDougall A, et al. Ca2+ oscillations promote APC/C-dependent cyclin B1 degradation during metaphase arrest and completion of meiosis in fertilizing mouse eggs. Curr Biol. 2002;12(9):746–750.
  • Yamamoto TM, Iwabuchi M, Ohsumi K, et al. APC/C–cdc20-mediated degradation of cyclin B participates in CSF arrest in unfertilized xenopus eggs. Dev Biol. 2005;279(2):345–355.
  • Oh JS, Susor A, Schindler K, et al. Cdc25A activity is required for the metaphase II arrest in mouse oocytes. J Cell Sci. 2013;126(5):1081–1085.
  • Oh JS, Susor A, Conti M. Protein tyrosine kinase Wee1B is essential for metaphase II exit in mouse oocytes. Science. 2011;332(6028):462–465.
  • Verlhac M-H, Lefebvre C, Kubiak JZ, et al. Mos activates MAP kinase in mouse oocytes through two opposite pathways. Embo J. 2000;19(22):6065–6074.
  • Verlhac MH, Kubiak JZ, Clarke HJ, et al. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development. 1994;120(4):1017–1025.
  • Clift D, Schuh M. Re-starting life: fertilization and the transition from meiosis to mitosis. Nat Rev Mol Cell Biol. 2013;14(9):549–562.
  • Strauss B, Harrison A, Coelho PA, et al. Cyclin B1 is essential for mitosis in mouse embryos, and its nuclear export sets the time for mitosis. J Cell Biol. 2018;217(1):179–193.
  • Jackman M, Firth M, Pines J. Human Cyclins B1 and B2 are localized to strikingly different structures: B1 to microtubules, B2 primarily to the golgi apparatus. Embo J. 1995;14(8):1646–1654.
  • Marangos P, Carroll J. The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction. 2004;128(2):153–162.
  • Holt JE, Weaver J, Jones KT. Spatial regulation of APCCdh1-induced cyclin B1 degradation maintains G2 arrest in mouse oocytes. Development. 2010;137(8):1297–1304.
  • Kotani T, Yasuda K, Ota R, et al. Cyclin B1 MRNA translation is temporally controlled through formation and disassembly of RNA granules. J Cell Biol. 2013;202(7):1041–1055.
  • Yang Y, Yang C-R, Han SJ, et al. Maternal MRNAs with Distinct 3′ UTRs define the temporal pattern of Ccnb1 synthesis during mouse oocyte meiotic maturation. Genes Dev. 2017;31(13):1302–1307.
  • Han SJ, Martins JPS, Yang Y, et al. The translation of cyclin B1 and B2 is differentially regulated during mouse oocyte reentry into the meiotic cell cycle. Sci Rep. 2017;7(1). DOI:10.1038/s41598-017-13688-3
  • Gui L, Homer H. Hec1-dependent cyclin B2 stabilization regulates the G2-M transition and early prometaphase in mouse oocytes. Dev Cell. 2013;25(1):43–54.
  • Rattani A, Vinod PK, Godwin J, et al. Dependency of the spindle assembly checkpoint on Cdk1 renders the anaphase transition irreversible. Curr Biol. 2014;24(6):630–637.
  • Touati SA, Buffin E, Cladière D, et al. Mouse oocytes depend on BubR1 for proper chromosome segregation but not for prophase I arrest. Nat Commun. 2015;6(April):6946.
  • Gallant P, Nigg EA. Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins. Embo J. 1994;13(3):595–605.
  • Sigrist S, Jacobs H, Stratmann R, et al. Exit from mitosis is regulated by drosophila fizzy and the sequential destruction of cyclins A, B and B3. Embo J. 1995;14(19):4827–4838.
  • Lozano J-C, Perret E, Schatt P, et al. Molecular cloning, gene localization, and structure of human cyclin B3. Biochem Biophys Res Commun. 2002;291(2):406–413.
  • Kreutzer MA, Richards JP, De Silva-Udawatta MN, et al. Caenorhabditis elegans cyclin A- and B-type genes: a cyclin A multigene family, an ancestral cyclin B3 and differential germline expression. J Cell Sci. 1995;108(Pt 6):2415–2424.
  • Lozano JC, Vergé V, Schatt P, et al. Evolution of cyclin B3 shows an abrupt three-fold size increase, due to the extension of a single exon in placental mammals, allowing for new protein-protein interactions. Mol Biol Evol. 2012;29:3855–3871.
  • Yuan K, O’Farrell PH. Cyclin B3 is a mitotic cyclin that promotes the metaphase-anaphase transition. Curr Biol. 2015;25:811–816.
  • Jacobs HW, Knoblich JA, Lehner CF. Drosophila cyclin B3 is required for female fertility and is dispensable for mitosis like cyclin B. Genes Dev. 1998;12(23):3741–3751.
  • Bourouh M, Dhaliwal R, Rana K, et al. Distinct and overlapping requirements for cyclins A, B and B3 in drosophila female meiosis. G3: Genes Genomes Genet. 2016;6:3711–3724.
  • Matthew MW. Cyclin CYB-3 controls both S-phase and mitosis and is asymmetrically distributed in the early C. Elegans Embryo. Development. 2016;143(17):3119–3127.
  • Deyter GMR, Furuta T, Kurasawa Y, et al. Caenorhabditis Elegans Cyclin B3 is required for multiple mitotic processes including alleviation of a spindle checkpoint–dependent block in anaphase chromosome segregation. PLoS Genet. 2010;6(11):e1001218.
  • Pierron G, Tirode F, Lucchesi C, et al. A new subtype of bone sarcoma defined by BCOR-CCNB3 gene fusion. Nat Genet. 2012;44(4):461–466.
  • Wan-Shan L, Chuang Liao I, Wen M-C, et al. BCOR-CCNB3-positive soft tissue sarcoma with round-cell and spindle-cell histology: a series of four cases highlighting the pitfall of mimicking poorly differentiated synovial sarcoma. Histopathology. 2016;69(5):792–801.
  • Cohen-Gogo S, Cellier C, Coindre J-M, et al. Ewing-like Sarcomas with BCOR-CCNB3 fusion transcript: a clinical, radiological and pathological retrospective study from the Société Française Des Cancers de L’Enfant. Pediatr Blood Cancer. 2014;61(12):2191–2198.
  • Voet MVD, Lorson MA, Srinivasan DG, et al. C. Elegans mitotic cyclins have distinct as well as overlapping functions in chromosome segregation. Cell Cycle. 2009;8(24):4091–4102.
  • Nguyen TB, Manova K, Capodieci P, et al. Characterization and expression of mammalian cyclin B3, a prepachytene meiotic cyclin. J Biol Chem. 2002;277(44):41960–41969.
  • Treen N, Heist T, Wang W, et al. Depletion of maternal cyclin B3 contributes to zygotic genome activation in the ciona embryo. Curr Biol. 2018;28(7):1150–1156.e4.
  • Zhang T, Qi ST, Huang L, et al. Cyclin B3 controls anaphase onset independent of spindle assembly checkpoint in meiotic oocytes. Cell Cycle. 2015;14(16):2648–2654.

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