Universal recipients in the G2 phase of mitotic cell cycle (preactivated oocytes, zygotes, blastomeres) accept embryonic nuclei in all the stages of their cell cycle. To test if recipients in the G2 of meiotic cycle (immature oocytes) are universal recipients, mouse germinal vesicle (GV) oocytes were enucleated and reconstructed with blastomere nuclei in the G1, S, or G2 stages. Analysis of their maturation has shown that about 30% of the G1 nuclei and 60% of G2 nuclei allow for normal metaphase II (MII), both in the oocytes with and without the first polar body (1st PB). Among oocytes reconstructed with the S phase nuclei, only 8% or less have normal MII, although 75% of them extrude 1st PB. No phase of donor cell cycle prevented the abnormal acceleration of 1st PB extrusion, found in reconstructed GV oocytes. In conclusion, enucleated GV oocytes are not universal recipients of embryonic nuclei, because they do not accept the S donors. However, both the G1 and G2 donor nuclei can be reprogrammed in the GV oocyte cytoplasm.
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References
1.
BoltonV.N., OadesP.J., JohnsonM.H.1984. The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryo. J. Embryol. Exp. Morphol., 79:139–163.
2.
BuiH.-T., WakayamaS., KishigamiS.et al.2008. The cytoplasm of mouse germinal vesicle stage oocytes can enhance somatic cell nuclear reprogramming. Development, 135:3935–3945.
3.
CampbellK.H.S., RitchieW.A., WilmutI.1993. Nuclear–cytoplasmic interactions during the first cell cycle of nuclear transfer reconstructed bovine embryos: implications for deoxyribonucleic acid replication and development. Biol. Reprod., 49:933–942.
4.
CampbellK.H.S., LoiP., CappaiP.et al.1994. Improved development to blastocyst of ovine nuclear transfer embryos reconstructed during the presumptive S-phase of enucleated activated oocytes. Biol. Reprod., 50:1385–1393.
5.
CampbellK.H.S., LoiP., OtaeguiP.J.et al.1996. Cell cycle co-ordination in embryo cloning by nuclear transfer. Rev. Reprod., 1:40–46.
6.
ChangC.C., NagyZ.P., AbdelmassihR.et al.2004. Nuclear and microtubule dynamics of G2/M somatic nuclei during haploidization in germinal vesicle-stage mouse oocytes. Biol. Reprod., 70:752–758.
7.
ChangC.C., NagyZ.P., AbdelmassihR.et al.2006. Interactions of the meiotic spindle with mitotic chromosomes in GV mouse oocytes. Reprod. Biomed. Online, 13:213–221.
8.
CheongH.T., TakahashiY., KanagawaH.1993. Birth of mice after transplantation of early-cell stage embryonic nuclei into enucleated oocytes. Biol. Reprod., 4:958–963.
9.
CiemerychM.A., MaroB., KubiakJ.Z.1999. Control of duration of the first two mitoses in a mouse embryo. Zygote, 7:293–300.
10.
CollasP., RoblJ.M.1991. Relationship between nuclear remodelling and development in nuclear transplant rabbit embryos. Biol. Reprod., 45:455–465.
11.
CollasP., Pinto-CorreiaC., Ponce de LeonF.A.et al.1992. Effect of donor cell cycle stage on chromatin and spindle morphology in nuclear transplant rabbit embryos. Biol. Reprod., 46:501–511.
12.
DulbeccoR., VogtM.1954. Plaque formation and isolation of pure lines with Poliomyelitis viruses. J. Exp. Med., 99:167–182.
13.
FulkaJ.Jr., MoorR.M., FulkaJ.1995. Replicating DNA does not block germinal vesicle breakdown in mouse oocytes. J. Exp. Zool., 272:245–248.
14.
FultonB.P., WhittinghamD.G.1978. Activation of mammalian oocytes by intracellular injection of calcium. Nature, 273:149–151.
15.
GrabarekJ.B., PlusaB., ModlinskiJ.A.et al.2004. Reconstruction of enucleated mouse germinal vesicle oocytes with blastomere nuclei. Zygote, 12:163–172.
16.
HomerH.A., McDougallA., LevasseurM.et al.2005. Mad2 prevents aneuploidy and premature proteolysis of cyclin B and securing during meiosis I in mouse oocytes. Genes Dev., 19:202–207.
17.
JohnsonR.T., RaoP.N., HughesH.D.1970. Mammalian cell fusion. 3. A Hela cell inducer of premature chromosome condensation active in cells from a variety of animal species. J. Cell. Physiol., 76:151–157.
18.
KitajimaT.S., KawashimaS.A., WatanabeY.2004. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature, 427:510–517.
19.
KouznetsovaA., ListerL., NordenskjoldM.et al.2007. Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat. Genet., 39:966–968.
20.
Lima-de-FariaA., BorumK.1962. The period of DNA synthesis prior to meiosis in the mouse. J. Cell. Biol., 14:381–388.
21.
MaltzmannW., CzyzykL.1994. UV irradiation stimulates levels of p53 cellular tumour antigen in non-transformed mouse cells. Mol. Cell Biol., 4:1689–1694.
22.
ModlinskiJ.A., GrabarekJ., PlusaB.et al.2001. The possible role of cell cycle stage in mammalian cloning. J. Appl. Genet., 42:153–176.
23.
MohammedA.A., KarasiewiczJ., ModlińskiJ.A.2008. Developmental potential of selectively enucleated immature mouse oocytes upon nuclear transfer. Mol. Reprod. Dev., 75:1269–1280.
24.
NanC.-L., OuyangY.-C., ZhaoZ.-J.et al.2007. Time course of meiotic progression after transferring primary spermatocyte into ooplasm at different stages. Mol. Reprod. Dev., 74:1072–1080.
25.
NiaultT., HachedK., SotilloR.et al.2007. Changing Mad2 levels affects chromosome segregation and spindle assembly checkpoint control in female mouse meiosis I. PLoS ONE, 2:e1165.
26.
PetersH., LevyE., CroneM.1962. Deoxyribonuclei acid synthesis in oocytes of mouse embryos. Nature, 195:915–916.
27.
PetronczkiM., SiomosM.F., NasmythK.2003. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell, 112:423–440.
PyrzynskaB., MaleszewskiM., MaluchnikD.1996. Mouse oocytes penetrated by sperm at GV or GVBD stage lose the ability to fuse with additional spermatozoa. Zygote, 4:123–128.
30.
SawickiW., AbramczukJ., BlatonO.1978. DNA synthesis in the second and third cell cycles of mouse preimplantation development. A cytophotometric study. Exp. Cell Res., 112:199–205.
31.
SchwartzA., CookP.R., HarrisH.1971. Correction of a genetic defect in a mammalian cell. Nature, 230:5–8.
32.
SluderG., McCollumD.2000. Molecular biology. The mad ways of meiosis. Science, 289:254–255.
33.
SmithL.C., WilmutI., HunterR.H.F.1988. Influence of cell cycle stage at nuclear transplantation on the development in vitro of mouse embryos. J. Reprod. Fertil., 84:619–624.
34.
SmithL.C., WilmutI., WestJ.D.1990. Control of first cleavage in single-cell reconstituted mouse embryos. J. Reprod. Fertil., 88:655–663.
35.
SmithR.K., JohnsonM.H.1986. Analysis of the third and fourth cell cycles of mouse early development. J. Reprod. Fertil., 76:393–399.
36.
TaniT., KatoY., TsunodaY.2007. Aberrant spindle assembly checkpoint in bovine somatic cell nuclear transfer oocytes. Front. Biosci., 12:2693–2705.
37.
TarkowskiA.K., WroblewskaJ.1967. Development of blastomeres of mouse eggs isolated at the 4- and 8-cell stage. J. Embryol. Exp. Morphol., 18:155–180.
38.
TelfordN.A., WatsonA.J., SchultzGA.1990. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev., 26:90–100.
39.
TsurumiC., HoffmannS., GeleyS.et al.2004. The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J. Cell. Biol., 167:1037–1050.
40.
WhittinghamD.G.1971. Culture of mouse ova. J. Reprod. Fertil. Suppl., 14:7–21.
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