Nucleologenesis and Nucleolotransfer in Mammalian Oocytes: A Review

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Abstract

An effort to improve development potential of early embryos is one of the main goals of biotechnology in the area of reproductive biology with application in veterinary or human medicine. Recent observations of the function of nucleolus or rather its forms before, during and after the fertilisation or parthenogenetic activation show the key role(s) of nucleolus in the processes of early genome activation. The nucleolus is a subnuclear structure (organelle) mainly involved in regulation of transcription and translation. This organelle has been characterized in detail by immunofluorescence, cell transfection and proteomics. This data was, however, mostly obtained in nucleoli of differentiated eukaryotic cells. Much less is known about the nucleolar structural changes and related functional processes in growing and fully grown mammalian oocytes, zygotes and early cleavage stage embryos, especially in the context of embryonic genome activation. It has been shown, that nucleoli in mammalian oocytes and early embryos have several forms and functions, which vary during the oocyte growth and embryonic development. Certain functions have not been fully described or explained, yet. The method of enucleolation, which allows to remove nucleoli from the oocytes or to exchange nucleoli between oocytes or zygotes, together with their proteomic and structural analyses brought new information about functions of nucleoli in oocytes and early cleavage-stage embryos and allowed to explain some new key roles of nucleoli during oocyte maturation and early embryonic development.

1. Fulka, H., Kyogoku, H., Zatsepina, O., Langerova, A, Fulka, J. Jr. (2015). Can nucleoli be markers of developmental potential in human zygotes? Trends Mol Med. 21 (11): 663–672. https://doi.org/10.1016/j.molmed.2015.09.005 PMid:26494190

2. Lefèvre, B. (2008). The nucleolus of the maternal gamete is essential for life. Bioessays 30, 613–616. https://doi.org/10.1002/bies.20774 PMid:18536024

3. Fulka, J. Jr., Moor, R. M., Loi, P., Fulka, J. (2003). Enucleolation of porcine oocytes. Theriogenology 59, 1879–1885. https://doi.org/10.1016/S0093-691X(02)01226-8

4. Rodman, T. C., Bachvarova, R. (1976). RNA synthesis in preovulatory mouse oocytes. J. Cell Biol. 70, 251–257. https://doi.org/10.1083/jcb.70.1.251 PMid:932101

5. Chouinard, L. A. (1975). A light- and electron-microscope study of the oocyte nucleus during development of the antral follicle in the prepubertal mouse. J. Cell Sci. 17, 589–615. PMid:1141388

6. Chouinard, L. A. (1971). A light- and electron-microscope study of the nucleolus during growth of the oocyte in the prepubertal mouse. J. Cell Sci. 9, 637–663. PMid:4112474

7. Fulka, H., Langerova, A. (2014). The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition. Development 141, 1694–1704. https://doi.org/10.1242/dev.105940 PMid:24715459

8. Kyogoku, H. Fulka, J. Jr., Wakayama, T., Miyano, T. (2014). De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes. Development 141, 2255–2259. https://doi.org/10.1242/dev.106948 PMid:24803589

9. Christians, E., Boiani, M., Garagna, S., Dessy, C., Redi, C. A., Renard, J. P., Zuccotti, M. (1999). Gene expression and chromatin organization during mouse oocyte growth. Dev Biol. 207 (1): 76–85. https://doi.org/10.1006/dbio.1998.9157 PMid:10049566

10. Bachant, J. B., Elledge, S. J. (1999). Cell cycle: Mitotic treasures in the nucleolus. Nature 398, 757–758. https://doi.org/10.1038/19641 PMid:10235256

11. Inoue, A. Nakajima, R., Nagata, M., Aoki, F. (2008). Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum. Reprod. 23, 1377–1384. https://doi.org/10.1093/humrep/den096 PMid:18367455

12. Fulka, H., Martinkova. S., Kyogoku, H., Langerova, A., Fulka, J. Jr. (2012). Production of giant mouse oocyte nucleoli and assessment of their protein content. J. Reprod. Dev. 58, 371–376. https://doi.org/10.1262/jrd.2011-004 PMid:22293324

13. Snustad, D. P., Simmons, M. J. (2009). Principles of genetics. John Wiley & Sons, UK, 18

14. Ogushi, S., Palmieri, C., Fulka, H., Saitou, M., Miyano, T., Fulka, J. Jr. (2008). The maternal nucleolus is essential for early embryonic development in mammals. Science 319, 613–616. https://doi.org/10.1126/science.1151276 PMid:18239124

15. Flechon, J. E., Kopecny, V. (1998). The nature of the ‚nucleolus precursor body‘ in early preimplantation embryos: a review of fine-structure cytochemical, immunocytochemical and autoradiographic data related to nucleolar function. Zygote 6, 183–191. https://doi.org/10.1017/S0967199498000112 PMid:9770784

16. Derenzini, M., Thiry, M., Goessens, G. (1990). Ultrastructural cytochemistry of the mammalian cell nucleolus. J. Histochem. Cytochem. 38, 1237–1256. https://doi.org/10.1177/38.9.2201735 PMid:2201735

17. Olson, M. O. J., Dundr, M., Szebeni, A. (2000). The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol. 10, 189–196. https://doi.org/10.1016/S0962-8924(00)01738-4

18. Schultz, R. M. (2002). The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Update. 8, 323–331. https://doi.org/10.1093/humupd/8.4.323 PMid:12206467.

19. Zatsepina, O., Baly, C., Chebrout, M., Debey, P. (2003). The step-wise assembly of a functional nucleolus in preimplantation mouse embryos involves the Cajal (coiled) body. Dev. Biol. 253, 66–83. https://doi.org/10.1006/dbio.2002.0865 PMid:12490198

20. Wakayama, T., Rodriguez, I., Perry, A. C., Yanagimachi, R., Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 96, 14984–14989. https://doi.org/10.1073/pnas.96.26.14984 PMid:10611324 PMCid:PMC24759

21. Wakayama, T., Yanagimachi, R. (2001). Mouse cloning with nucleus donor cells of different age and type. Mol. Reprod. Dev. 58, 376–383. https://doi.org/10.1002/1098-2795(20010401)58:4<376::AID-MRD4>3.0.CO;2-L

22. Ogushi, S., Saitou, M. (2010). The nucleolus in the mouse oocyte is required for the early step of both female and male pronucleus organization. J. Reprod. Dev. 56, 495–501. https://doi.org/10.1262/jrd.09-184H PMid:20519829

23. Hernandez-Verdun, D., Roussel, P., Thiry, M., Sirri, V., Lafontaine, D. L. (2010). The nucleolus: structure/function relationship in RNA metabolism. Wiley Interdiscip Rev RNA. 1 (3): 415–431. https://doi.org/10.1002/wrna.39 PMid:21956940

24. Koolman, J., Röhm, K. H. (2009). Taschenatlas biochemie des menschen. Georg Thieme Verlag Stuttgart, New York, 66. https://doi.org/10.1055/b-002-15439

Macedonian Veterinary Review

The Journal of the Faculty of Veterinary Medicine-Skopje at the Ss. Cyril and Methodius University in Skopje

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