Increased Expression of Maturation Promoting Factor Components Speeds Up Meiosis in Oocytes from Aged Females

. 2018 Sep 19 ; 19 (9) : . [epub] 20180919

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30235877

Grantová podpora
EXCELLENCECZ.02.1.01/0.0/0.0/15_003/0000460 OP RDE, GACR18-19395S, GACR15-22765S, MC EIF - 708255, GACR18-02891S, Institutional Research Concept RVO67985904 MSMT, GACR, MC EIF

The rate of chromosome segregation errors that emerge during meiosis I in the mammalian female germ line are known to increase with maternal age; however, little is known about the underlying molecular mechanism. The objective of this study was to analyze meiotic progression of mouse oocytes in relation to maternal age. Using the mouse as a model system, we analyzed the timing of nuclear envelope breakdown and the morphology of the nuclear lamina of oocytes obtained from young (2 months old) and aged females (12 months old). Oocytes obtained from older females display a significantly faster progression through meiosis I compared to the ones obtained from younger females. Furthermore, in oocytes from aged females, lamin A/C structures exhibit rapid phosphorylation and dissociation. Additionally, we also found an increased abundance of MPF components and increased translation of factors controlling translational activity in the oocytes of aged females. In conclusion, the elevated MPF activity observed in aged female oocytes affects precocious meiotic processes that can multifactorially contribute to chromosomal errors in meiosis I.

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Colegrove-Otero L.J., Devaux A., Standart N. The Xenopus ELAV protein ElrB represses Vg1 mRNA translation during oogenesis. Mol. Cell. Biol. 2005;25:9028–9039. doi: 10.1128/MCB.25.20.9028-9039.2005. PubMed DOI PMC

Schuh M., Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007;130:484–498. doi: 10.1016/j.cell.2007.06.025. PubMed DOI

Hassold T., Jacobs P., Kline J., Stein Z., Warburton D. Effect of maternal age on autosomal trisomies. Ann. Hum. Genet. 1980;44:29–36. doi: 10.1111/j.1469-1809.1980.tb00943.x. PubMed DOI

Pan H., Ma P., Zhu W., Schultz R.M. Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev. Biol. 2008;316:397–407. doi: 10.1016/j.ydbio.2008.01.048. 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

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

Hunt P. Oocyte Biology: Do the Wheels Fall Off with Age? Curr. Biol. 2017;27:R266–R269. doi: 10.1016/j.cub.2017.02.035. PubMed DOI

Chiang T., Duncan F.E., Schindler K., Schultz R.M., Lampson M.A. Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr. Biol. 2010;20:1522–1528. doi: 10.1016/j.cub.2010.06.069. PubMed DOI PMC

Merriman J.A., Jennings P.C., McLaughlin E.A., Jones K.T. Effect of aging on superovulation efficiency, aneuploidy rates, and sister chromatid cohesion in mice aged up to 15 months. Biol. Reprod. 2012;86 doi: 10.1095/biolreprod.111.095711. PubMed DOI

Chiang T., Schultz R.M., Lampson M.A. Meiotic Origins of Maternal Age-Related Aneuploidy. Biol. Reprod. 2012;86 doi: 10.1095/biolreprod.111.094367. PubMed DOI PMC

Dechat T., Pfleghaar K., Sengupta K., Shimi T., Shumaker D.K., Solimando L., Goldman R.D. Nuclear lamins: Major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 2008;22:832–853. doi: 10.1101/gad.1652708. PubMed DOI PMC

Heald R., McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell. 1990;61:579–589. doi: 10.1016/0092-8674(90)90470-Y. PubMed DOI

Susor A., Jansova D., Cerna R., Danylevska A., Anger M., Toralova T., Malik R., Supolikova J., Cook M.S., Oh J.S., et al. Temporal and spatial regulation of translation in the mammalian oocyte via the mTOR-eIF4F pathway. Nat. Commun. 2015;6 doi: 10.1038/ncomms7078. PubMed DOI PMC

Sanfins A., Plancha C.E., Overstrom E.W., Albertini D.F. Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: Insights into the relationship between nuclear and cytoplasmic quality. Hum. Reprod. 2004;19:2889–2899. doi: 10.1093/humrep/deh528. PubMed DOI

Haithcock E., Dayani Y., Neufeld E., Zahand A.J., Feinstein N., Mattout A., Gruenbaum Y., Liu J. Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 2005;102:16690–16695. doi: 10.1073/pnas.0506955102. PubMed DOI PMC

Righolt C.H., van ’t Hoff M.L.R., Vermolen B.J., Young I.T., Raz V. Robust nuclear lamina-based cell classification of aging and senescent cells. Aging. 2011;3:1192–1201. doi: 10.18632/aging.100414. PubMed DOI PMC

Adhikari D., Zheng W., Shen Y., Gorre N., Ning Y., Halet G., Kaldis P., Liu K. Cdk1, but not Cdk2, is the sole Cdk that is essential and sufficient to drive resumption of meiosis in mouse oocytes. Hum. Mol. Genet. 2012;21:2476–2484. doi: 10.1093/hmg/dds061. PubMed DOI

Peter M., Nakagawa J., Dorée M., Labbé J.C., Nigg E.A. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell. 1990;61:591–602. doi: 10.1016/0092-8674(90)90471-P. PubMed DOI

Jones K.T. Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization. Mol. Hum. Reprod. 2004;10:1–5. doi: 10.1093/molehr/gah009. PubMed DOI

Morgan D.O. Principles of CDK regulation. Nature. 1995;374:131–134. doi: 10.1038/374131a0. PubMed DOI

Ducommun B., Brambilla P., Félix M.A., Franza B.R., Karsenti E., Draetta G. cdc2 phosphorylation is required for its interaction with cyclin. EMBO J. 1991;10:3311–3319. doi: 10.1002/j.1460-2075.1991.tb04895.x. PubMed DOI PMC

Solomon M.J. Activation of the various cyclin/cdc2 protein kinases. Curr. Opin. Cell Biol. 1993;5:180–186. doi: 10.1016/0955-0674(93)90100-5. PubMed DOI

Hampl A., Eppig J.J. Translational regulation of the gradual increase in histone H1 kinase activity in maturing mouse oocytes. Mol. Reprod. Dev. 1995;40:9–15. doi: 10.1002/mrd.1080400103. PubMed DOI

Lévesque J.T., Sirard M.A. Resumption of meiosis is initiated by the accumulation of cyclin B in bovine oocytes. Biol. Reprod. 1996;55:1427–1436. doi: 10.1095/biolreprod55.6.1427. PubMed DOI

Davydenko O., Schultz R.M., Lampson M.A. Increased CDK1 activity determines the timing of kinetochore-microtubule attachments in meiosis I. J. Cell Biol. 2013;202:221–229. doi: 10.1083/jcb.201303019. PubMed DOI PMC

Rieder C.L. The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma. 1981;84:145–158. doi: 10.1007/BF00293368. PubMed DOI

Eichenlaub-Ritter U., Boll I. Age-related non-disjunction, spindle formation and progression through maturation of mammalian oocytes. Prog. Clin. Biol. Res. 1989;318:259–269. PubMed

Zuccotti M., Boiani M., Garagna S., Redi C.A. Analysis of aneuploidy rate in antral and ovulated mouse oocytes during female aging. Mol. Reprod. Dev. 1998;50:305–312. doi: 10.1002/(SICI)1098-2795(199807)50:3<305::AID-MRD6>3.0.CO;2-N. PubMed DOI

Liu L., Keefe D.L. Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice. Hum. Reprod. 2002;17:2678–2685. doi: 10.1093/humrep/17.10.2678. PubMed DOI

Cukurcam S., Betzendahl I., Michel G., Vogt E., Hegele-Hartung C., Lindenthal B., Eichenlaub-Ritter U. Influence of follicular fluid meiosis-activating sterol on aneuploidy rate and precocious chromatid segregation in aged mouse oocytes. Hum. Reprod. 2007;22:815–828. doi: 10.1093/humrep/del442. PubMed DOI

Chiang T., Schultz R.M., Lampson M.A. Age-Dependent Susceptibility of Chromosome Cohesion to Premature Separase Activation in Mouse Oocytes. Biol. Reprod. 2011;85:1279–1283. doi: 10.1095/biolreprod.111.094094. PubMed DOI PMC

Eichenlaub-Ritter U., Chandley A.C., Gosden R.G. The CBA mouse as a model for age-related aneuploidy in man: Studies of oocyte maturation, spindle formation and chromosome alignment during meiosis. Chromosoma. 1988;96:220–226. doi: 10.1007/BF00302361. PubMed DOI

Eichenlaub-Ritter U., Boll I. Nocodazole sensitivity, age-related aneuploidy, and alterations in the cell cycle during maturation of mouse oocytes. Cytogenet. Genome Res. 1989;52:170–176. doi: 10.1159/000132871. PubMed DOI

Duncan F.E., Chiang T., Schultz R.M., Lampson M.A. Evidence That a Defective Spindle Assembly Checkpoint Is Not the Primary Cause of Maternal Age-Associated Aneuploidy in Mouse Eggs1. Biol. Reprod. 2009;81:768–776. doi: 10.1095/biolreprod.109.077909. PubMed DOI PMC

Lister L.M., Kouznetsova A., Hyslop L.A., Kalleas D., Pace S.L., Barel J.C., Nathan A., Floros V., Adelfalk C., Watanabe Y., et al. Age-Related Meiotic Segregation Errors in Mammalian Oocytes Are Preceded by Depletion of Cohesin and Sgo2. Curr. Biol. 2010;20:1511–1521. doi: 10.1016/j.cub.2010.08.023. PubMed DOI

Cui L.-B., Zhou X.-Y., Zhao Z.-J., Li Q., Huang X.-Y., Sun F.-Z. The Kunming mouse: As a model for age-related decline in female fertility in human. Zygote. 2013;21:367–376. doi: 10.1017/S0967199412000123. PubMed DOI

Gui L., Homer H. Hec1-dependent cyclin B2 stabilization regulates the G2-M transition and early prometaphase in mouse oocytes. Dev. Cell. 2013;25:43–54. doi: 10.1016/j.devcel.2013.02.008. PubMed DOI PMC

De Smedt V., Poulhe R., Cayla X., Dessauge F., Karaiskou A., Jessus C., Ozon R. Thr-161 phosphorylation of monomeric Cdc2. Regulation by protein phosphatase 2C in Xenopus oocytes. J. Biol. Chem. 2002;277:28592–28600. doi: 10.1074/jbc.M202742200. PubMed DOI

Félix M.A., Cohen P., Karsenti E. Cdc2 H1 kinase is negatively regulated by a type 2A phosphatase in the Xenopus early embryonic cell cycle: Evidence from the effects of okadaic acid. EMBO J. 1990;9:675–683. doi: 10.1002/j.1460-2075.1990.tb08159.x. PubMed DOI PMC

Li J., Tang J.-X., Cheng J.-M., Hu B., Wang Y.-Q., Aalia B., Li X.-Y., Jin C., Wang X.-X., Deng S.-L., et al. Cyclin B2 can compensate for Cyclin B1 in oocyte meiosis I. J. Cell Biol. 2018 doi: 10.1083/jcb.201802077. PubMed DOI PMC

Duncan F.E., Jasti S., Paulson A., Kelsh J.M., Fegley B., Gerton J.L. Age-associated dysregulation of protein metabolism in the mammalian oocyte. Aging Cell. 2017;16:1381–1393. doi: 10.1111/acel.12676. PubMed DOI PMC

Xue S., Barna M. Specialized ribosomes: A new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 2012;13:355–369. doi: 10.1038/nrm3359. PubMed DOI PMC

Tao X., Landis J.N., Krisher R.L., Duncan F.E., Silva E., Lonczak A., Scott R.T., Zhan Y., Chu T., Scott R.T., et al. Mitochondrial DNA content is associated with ploidy status, maternal age, and oocyte maturation methods in mouse blastocysts. J. Assist. Reprod. Genet. 2017;34:1587–1594. doi: 10.1007/s10815-017-1070-8. PubMed DOI PMC

Fragouli E., Spath K., Alfarawati S., Kaper F., Craig A., Michel C.-E., Kokocinski F., Cohen J., Munne S., Wells D. Altered Levels of Mitochondrial DNA Are Associated with Female Age, Aneuploidy, and Provide an Independent Measure of Embryonic Implantation Potential. PLoS Genet. 2015;11 doi: 10.1371/journal.pgen.1005241. PubMed DOI PMC

Raz V., Vermolen B.J., Garini Y., Onderwater J.J.M., Mommaas-Kienhuis M.A., Koster A.J., Young I.T., Tanke H., Dirks R.W. The nuclear lamina promotes telomere aggregation and centromere peripheral localization during senescence of human mesenchymal stem cells. J. Cell. Sci. 2008;121:4018–4028. doi: 10.1242/jcs.034876. PubMed DOI

Maiato H., Hergert P.J., Moutinho-Pereira S., Dong Y., Vandenbeldt K.J., Rieder C.L., McEwen B.F. The ultrastructure of the kinetochore and kinetochore fiber in Drosophila somatic cells. Chromosoma. 2006;115:469–480. doi: 10.1007/s00412-006-0076-2. PubMed DOI PMC

Schweizer N., Pawar N., Weiss M., Maiato H. An organelle-exclusion envelope assists mitosis and underlies distinct molecular crowding in the spindle region. J. Cell Biol. 2015;210:695–704. doi: 10.1083/jcb.201506107. PubMed DOI PMC

Katsani K.R., Karess R.E., Dostatni N., Doye V. In vivo dynamics of Drosophila nuclear envelope components. Mol. Biol. Cell. 2008;19:3652–3666. doi: 10.1091/mbc.e07-11-1162. PubMed DOI PMC

Tetkova A., Hancova M. Mouse Oocyte Isolation, Cultivation and RNA Microinjection. Bio-Protocol. 2016;6 doi: 10.21769/BioProtoc.1729. DOI

McGuinness B.E., Anger M., Kouznetsova A., Gil-Bernabé A.M., Helmhart W., Kudo N.R., Wuensche A., Taylor S., Hoog C., Novak B., et al. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr. Biol. 2009;19:369–380. doi: 10.1016/j.cub.2009.01.064. PubMed DOI

Eden E., Lipson D., Yogev S., Yakhini Z. Discovering Motifs in Ranked Lists of DNA Sequences. PLoS Comput. Biol. 2007;3:e39. doi: 10.1371/journal.pcbi.0030039. PubMed DOI PMC

Eden E., Navon R., Steinfeld I., Lipson D., Yakhini Z. GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinform. 2009;10:48. doi: 10.1186/1471-2105-10-48. PubMed DOI PMC

Motlík J., Sutovský P., Kalous J., Kubelka M., Moos J., Schultz R.M. Co-culture with pig membrana granulosa cells modulates the activity of cdc2 and MAP kinase in maturing cattle oocytes. Zygote. 1996;4:247–256. doi: 10.1017/S0967199400003166. PubMed DOI

Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. PubMed DOI

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