Abstract
Two forms of oocytes termed SN (Surrounded Nucleolus) and NSN (Non Surrounded Nucleolus) differing for the spatial distribution of nuclear and nucleolar-associated chromatin have been described within the antral compartment of the ovary of a number of mammals. The biological significance of these two kinds of oocytes is as yet not completely clear. In previous studies we have shown that prior to ovulation, SN oocytes isolated from the antral compartment, cultured and fertilizedin vitro (IVM-IVF) have a far better meiotic and developmental competence than NSN oocytes. Following ovulation the proportion of SN antral oocytes diminishes and those SN and NSN oocytes that remain in the antral compartment are uncapable of embryonic development beyond the 2-cell stage. To further examine the correlation between chromatin distribution and meiotic competence of mouse antral oocytes, in the present study we have analyzed chromosome segregation at the time of first meiotic division in SN and NSN antral oocytes and in ovulated oocytes. SN and NSN antral oocytes were isolated before (48 hr post PMSG injection) or after (15 hr post hCG injection) ovulation from ovaries of females of increasing age, they were culturedin vitro to metaphase II, and their aneuploidy rate was examined. Comparison of data obtained before and after ovulation highlights two main points: 1) following ovulation a statistically significant increase of aneuploidy is observed in antral oocytes in most age groups. This increase is mainly attributable to SN oocytes, whereas the aneuploidy rate in the group of NSN oocytes does not significantly change before and after ovulation. 2) The aneuploidy rate of MII ovulated oocytes has a decreasing trend during female aging. These results suggest that in the ovarian dynamics, SN antral oocytes may be favoured in the selection for ovulation.
Riassunto
Gli oociti antrali di tutti i Mammiferi studiati possono essere classificati in due categorie e denominati SN (Surrounded Nucleolus) o NSN (Non Surrounded Nucleolus) in base alla distribuzione della cromatina nucleare e perinucleolare. Il significato biologico di questi due tipi di oociti non è ancora completamente chiaro. In studi precedenti abbiamo dimostrato che oociti SN di topo isolati prima dell’ovulazione, possedevano una migliore competenza meiotica ed erano in grado di meglio procedere nello sviluppo embrionale degli oociti di tipo NSN. Se però gli oociti venivano isolati successivamente alla ovulazione, allora entrambi i due tipi di oociti erano incapaci di proseguire lo sviluppo embrionale oltre lo stadio di 2 cellule. Per capire meglio questa correlazione tra organizzazione della cromatina e competenza meiotica degli oociti antrali di topo, in questo studio abbiamo analizzato la segregazione cromosomica durante la prima divisione meiotica in oociti SN, NSN ed oociti ovulati di topo. Oociti SN e NSN sono stati isolati prima (48 ore post iniezione di PMSG) o dopo (15 ore post iniezione di hCG) l’ovulazione da ovari di femmine di età crescente, gli oociti sono quindi stati coltivatiin vitro fino alla metafase II, ed è stato analizzato il grado di aneuploidie. Il confronto tra i dati ottenuti prima e dopo l’ovulazione evidenzia due punti principali: 1) successivamente all’ovulazione è osservabile un aumento statisticamente significativo di aneuploidie negli oociti antrali in tutti i gruppi d’età analizzati. Questo aumento è principalmente attribuibile agli oociti di tipo SN, mentre il tasso di aneuploidie nel gruppo di oociti NSN non aumenta significativamente. 2) Il tasso di aneuploidie degli oociti ovulati diminuisce con l’età della femmina. Questi risultati suggeriscono che gli oociti antrali SN sono favoriti nella selezione per l’ovulazione.
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References
Antonarakis S. E., Peterson M. B., McInnis M. G., Adelsberger P. A., Schinzel A. A., Binkert F., Pangalos C., Raoul O., Salugherhaupt S. A., Hafets M., Cohen M., Roulsen D., Schwartz S., Mikkelsen M., Tranebjaerg L., Greenberg F., Hoar D., Rudd N. L., Warren A. C., Metaxotou C., Bartsocas C., Chakravarti A., 1992.The meiotic stage of nondisjunction in trisomy 21: determination by using DNA polymorphisms. Am. J. Hum. Genet., 50: 544–550.
Asakawa T., Ishikawa M., Shimizu M., Dukelow W. R., 1988.The chromosomal normality of in vitrofertilized rabbit oocytes. Biol. Reprod., 38: 292–295.
Bailey N. T. J., 1959.Simple significance tests based on the normal distribution. In:N. T. J. Bailey (ed.),Statistical methods in biology. Unibooks, English University Press, London: 33–42.
Brook J. D., Gosden R. G., Chandley A. C., 1984.Maternal aging and aneuploid embryos — Evidence from the mouse that biological age and not chronological age is the important influence. Human Genet., 66: 41–45.
Crozet N., Motlik J., Szollosi D., 1981.Nuclear fine structure and RNA synthesis in porcine oocytes during early stages of antrum formation. Biol. Cell, 41: 35–42.
Crozet N., Kanka J., Motlik J., Fulka J., 1986.Nuclear fine structure and RNA synthesis in bovine oocytes from antral follicles. Gamete Res., 14: 65–73.
Debey P., Renard J. P., Coppey-Moisan M., Monnot I., Geze M., 1989.Dynamics of chromatin changes in live one-cell mouse embryos: a continuous follow-up by fluorescence microscopy. Exp. Cell Res., 183: 413–433.
Debey P., Szollosi M. S., Szollosi D., Vautier D., Girouse A., Besombes D., 1993.Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol. Reprod. Dev., 36: 59–74.
Fulton B. P., Whittingham D. G., 1978.Activation of mammalian oocytes by intracellular injection of calcium. Nature, 273: 149–151.
Garagna S., Zuccotti M., Giorgi Rossi P., Redi C. A., 1995.Organizzazione della cromatina in oociti antrali di topo durante la follicologenesi. Rend. Ist. Lomb., B 129: 93–107.
Golbus M. S., 1981.The influence of strain, maternal age, and method on mouse oocyte aneuploidy. Cytogenet. Cell Genet., 31: 84–90.
Hansmann I., Pabst B., 1992.Nondisjunction by failures in the molecular control of oocyte maturation. Ann. Anat., 174: 485–490.
Hansmann I., Beermann F., Hummler E., Theuring F., 1990.Aneuploidy in man and mechanism of nondisjunction inferred from studying Djungarian Hamster oocytes. In:T. Sharma (ed.),Trends in Chromosome Research. Springer-Verlag, Berlin-New York: 165–189.
Hassold T., 1985.The origin of aneuploidy in humans. In:V. L. Dellarco, P. E. Voytek, A. Hollaender (eds.),Aneuploidy — Etiology and Mechanisms. Plenum Press, New York-London: 103–115.
Hassold T., Chiu D., 1985.Maternal age-specific rates of numerical chromosome abnormalities with specifical reference to trisomy. Human Genet., 70: 11–17.
Hassold T., Jacobs P., 1984.Trisomy in man. Annual Review of Genetics, 18: 69–97.
King W. A., Desjardin M., Xu K. P., Bousquet D., 1990.Chromosome analysis of horse oocytes cultured in vitro. Genetic Sel Evol., 22: 151–160.
Mandl A. M., 1962.Pre-ovulatory changes in the oocyte of the adult rat. Proc. R. Soc. London (Biol.), 158: 105–118.
Martin R. H., Mahadevan M. M., Taylor P. J., 1986.Chromosomal analysis of unfertilized human oocytes. J. Reprod. Fertil., 78: 673–678.
Martin R. H., Ko E., Rademaker A., 1991.Distribution of aneuploidy in human gametes: comparison between human sperm and oocytes. Am. J. Med. Genet., 39: 321–331.
Mattson B. A., Albertini D. F., 1990.Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol. Reprod. Dev., 25: 374–383.
Parfenov V., Potchukalina G., Dudina L., Kostyucheck D., Gruzova M., 1989.Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). Gamete Res., 22: 219–231.
Plachot M., 1995.Oocyte — Genetic aspects. In:J. G. Grudzinskas, J. L. Yovich (eds.),Gametes. The oocyte. Cambridge University Press: 95–107.
Sorensen R. A., Wassarman P. M., 1976.Relationship between growth and meiotic maturation of the mouse oocyte. Dev. Biol., 50: 531–536.
Takagi N., Sasaki M., 1976.Digynic triploidy after superovulation in mice. Nature, 264: 278–281.
Tarkowski A. K., 1966.An air-drying method for chromosome preparation from mouse eggs. Cytogenetics, 5: 394–400.
Tilly J. L., Kowalski K. I., Johnson A. L., Hsueh A. J. W., 1990.Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology, 129: 2799–2801.
Wickramasinghe D., Ebert K. M., Albertini D. F., 1991.Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev. Biol., 143: 162–172.
Whittingham D. G., 1971.Colture of mouse ova. J. Reprod. Fertil. Suppl., 14: 7–21.
Zakowsky J. L., Martin Deleon P. A., 1988.Second meiotic nondisjunction is not increased in post-ovulatory aged murine oocytes fertilized in vitro. In Vitro Cell. Dev. Biol., 24: 133–137.
Zuccotti M., Piccinelli A., Giorgi Rossi P., Garagna S., Redi C. A., 1995.Chromatin organization during mouse oocyte growth. Mol. Reprod. Dev., 41: 479–485.
Zuccotti M., Giorgi Rossi P., Martinez A., Garagna S., Forabosco A., Redi C. A., 1998.Meiotic and developmental competence of mouse antral oocytes. Biol. Reprod., 58: 700–704.
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Nella seduta del 24 aprile 1998.
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Zuccotti, M., Boiani, M., Garagna, S. et al. Chromatin organization and meiotic non-disjunction in mouse oocytes. Rend. Fis. Acc. Lincei 9, 227–240 (1998). https://doi.org/10.1007/BF02904406
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DOI: https://doi.org/10.1007/BF02904406