Review Article
The oocyte´s nucleolus precursor body: The globe for life
Michal Benc * ,
Lazo Pendovski ,
Matej Murin ,
Frantisek Strejcek ,
Martin Morovic ,
Radek Prochazka ,
Jozef Laurincik

Mac Vet Rev 2018; 41 (2): 115 - 122

10.2478/macvetrev-2018-0013

Received: 28 November 2017

Received in revised form: 27 January 2018

Accepted: 12 February 2018

Available Online First: 31 March 2018

Published on: 15 October 2018

Correspondence: Michal Benc, benc.michal@gmail.com
PDF HTML

Abstract

The nucleolus is the cell organelle responsible for ribosome synthesis and, hence, for protein synthesis. In the mammalian oocyte, the nucleolus compacts into a dense sphere with no ribosome synthesis well in advance of ovulation. It seems, that this body is of utmost importance for the development of the embryo. It is unknown, however, how it exerts this essential function. During the last two decades, great attention has been paid to the study of nucleogenesis in oocytes and early embryos, with transcription of ribosomal DNA being evaluated as one of the criteria of normal development. In this review, we summarize some aspects of nucleolus transformation during oocyte growth, as well as during early embryonic development with possible impact on the quality of the embryos used in biomedical research. This knowledge in connection with further observations will substantially contribute to the development of new criteria suitable for evaluation of oocytes and embryos used in biomedical application.

Keywords: nucleolus precursor body, oocyte, embryo, transcriptomics, epigenetics


References

1. Hyttel, P., Fair, T., Callesen, H., Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23-32. https://doi.org/10.1016/S0093-691X(96)00336-6
2. Fair, T., Hyttel, P., Greve, T., Boland, M. (1996). Nucleolus structure and transcriptional activity in relation to oocyte diameter in cattle. Mol. Reprod. Dev. 43, 503-512.
https://doi.org/10.1002/(SICI)1098-2795(199604)43:4<503::AID-MRD13>3.0.CO;2-#
3. Bjerregaard, B., Wrenzycki, C., Philimonenko, V. V., Hozak, P., Laurincik, J., Niemann, H., Motlik, J., Maddox-Hyttel, P. (2003). Regulation of ribosomal RNA synthesis during the final phases of porcine oocyte growth. Biol. Reprod. 70, 925-935. https://doi.org/10.1095/biolreprod.103.020941 PMid:14627545
4. Hyttel, P., Laurincik, J., Rosenkranz, C., Rath, D., Niemann, H., Ochs, R. L., Schellander, K. (2000). Nucleolar proteins and ultrastructure in pre-implantation porcine embryos developed in vivo. Biol. Reprod. 63, 1848-1856. https://doi.org/10.1095/biolreprod63.6.1848 PMid:11090457
5. Laurincik, J., Thomsen, P.D., Hay-Schmidt, A., Avery, B., Greve, T., Ochs, R. L., Hyttel, P. (2000). Nucleolar proteins and nuclear ultrastructure in pre-implantation bovine embryos produced in vitro. Biol. Reprod. 62, 1024-1032. https://doi.org/10.1095/biolreprod62.4.1024 PMid:10727273
6. Bjerregaard, B., Wrenzycki, C., Strejcek, F., Laurincik, J., Holm, P., Ochs, R. L., Rosenkranz, C., Callesen, H., Rath, D., Niemann, H., Maddox-Hyttel, P. (2004). Expression of nucleolar related proteins in porcine preimplantation embryos produced in vivo and in vitro. Biol. Reprod. 70, 867-876. https://doi.org/10.1095/biolreprod.103.021683 PMid:14585813
7. Maddox-Hyttel, P., Bjerregaard, B., Laurincik, J. (2005). Meiosis and embryo technology:renaissance of the nucleolus. Reprod Fertil Dev. 17, 3-14. https://doi.org/10.1071/RD04108 PMid:15745627
8. Maddox-Hyttel, P., Svarcova, O., Laurincik, J. (2007). Ribosomal RNA and nucleolar proteins from the oocyte are to some degree used for embryonic nucleolar formation in cattle and pig. Theriogenology 68, 63-70. https://doi.org/10.1016/j.theriogenology.2007.03.015 PMid:17466364
9. Kyogoku, H., Ogushi, S., Miyano, T., Fulka, J. Jr. (2011). Nucleoli from growing oocytes inhibit the maturation of enucleolated, full-grown oocytes in the pig. Mol. Reprod. Dev. 78, 426-435. https://doi.org/10.1002/mrd.21320 PMid:21542050
10. Ogushi, S., Palmieri, Ch., 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
11. Wachtler, F., Stahl, A. (1993). The nucleolus:A structural and functional interpretation. Micron 24, 473-505. https://doi.org/10.1016/0968-4328(93)90026-W
12. Biggiogera, M., Malatesta, M., Abolhassani-Dadras, S., Amalric, F., Rothblum, L. I., Fakan, S. (2001). Revealing the unseen:the organizer region of the nucleolus. J. Cell Sci. 114, 3199–3205. PMid:11590246
13. Koberna, K., Malinsky, J., Pliss, A., Masata, M., Vecerova, J., Fialova, M., Bednar, J., Raska, I. (2002). Ribosomal genes in focus:new transcripts label the dense fibrillar components and form clusters indicative of “Christmas trees“in situ. J. Cell. Biol. 157, 743-748. https://doi.org/10.1083/jcb.200202007 PMid:12034768 PMCid:PMC2173423
14. Hozak, P., Cook, P. R., Schofer, C., Mosgoeller, W., Wachtler, F. (1994). Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. J. Cell Sci. 107, 639-648. PMid:8207086
15. Boisvert, F. M., Van Koningsbruggen, S., Navascues, J., Lamond, A. I. (2007). The multifunctional nucleolus. Nature 8, 574-585. https://doi.org/10.1038/nrm2184
16. Fulka, H., Fulka, J. Jr. (2010). Nucleolar transplantation in oocytes and zygotes:challenges for further research. Mol. Hum. Reprod. 16, 63-67. https://doi.org/10.1093/molehr/gap088 PMid:19819895
17. Crozet, N., Motlik, J., Szollosi, D. (1981). Nucleolar fine structure and RNA synthesis in porcine oocytes during early stages of antrum formation. Biol. Cell. 41, 35-42.
18. Motlik, J., Crozet, N., Fulka, J. (1984). Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J. Reprod. Fertil. 72, 323-328. https://doi.org/10.1530/jrf.0.0720323 PMid:6392543
19. Kopecny, V., Biggiogera, M., Laurincik, J., Pivko, J., Grafenau, P., Martin, T.E., Luhrmann, R., Fu, X. D., Fakan, S. (1996). Fine structural cytochemical and immunocytochemical analysis of nucleic acids and ribonucleoprotein distribution in nuclei of pig oocytes and early preimplantation embryos. Chromosoma 104, 561-574. https://doi.org/10.1007/BF00352296 PMid:⇖249
20. Kopecny, V., Landa, V., Pavlok, A. (1995). Localization of nucleic acids in the nucleoli of oocytes and early embryos of mouse and hamster:an autoradiographic study. Mol Reprod. Dev. 41 (4):449-458. https://doi.org/10.1002/mrd.1080410407 PMid:7576612
21. Bouniol-Baly, C., Hamraoui, L., Guibert, J., Beaujean, N., Szollosi, M. S., Debey, P. (1999). Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. Biol. Reprod. 60, 580-587. https://doi.org/10.1095/biolreprod60.3.580 PMid:10026102
22. De La Fuente, R. (2006). Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev. Biol. 292, 1-12. https://doi.org/10.1016/j.ydbio.2006.01.008 PMid:16466710
23. Fulka, H., Novakova, Z., Mosko, T., Fulka, J. Jr. (2009). The inability of fully grown germinal vesicle stage oocyte cytoplasm to transcriptionally silence transferred transcribing nuclei. Histochem Cell Biol. 132, 457-468. https://doi.org/10.1007/s00418-009-0625-x PMid:19649647
24. Andersen, J. S., Lam, Y. W., Leung, A. K. L., Ong, S., Lyon, C. E., Lamond, A. I., Mann, M. (2005). Nucleolar proteome dynamics. Nature 433, 77-82. https://doi.org/10.1038/nature03207 PMid:15635413
25. Ogushi, S., Yamagata, K., Obuse, C., Furuta, K., Wakayama, T., Matzuk, M. M., Saitou, M. (2017). Reconstitution of the oocyte nucleolus in mice through a single nucleolar protein, NPM2. J Cell Sci. 130, 2416-2429. https://doi.org/10.1242/jcs.195875 PMid:2↘324
26. Shishova, K. V., Lavrentyeva, E. A., Dobrucki, J. W., Zatsepina, O. V. (2015). Nucleolus-like bodies of fully-grown mouse oocytes contain key nucleolar proteins but are impoverished for rRNA. Dev. Biol. 397, 267-281. https://doi.org/10.1016/j.ydbio.2014.11.022 PMid:25481757
27. Bai, B., Liu, H., Laiho, M. (2014). Small RNA expression and deep sequencing analyses of the nucleolus reveal the presence of nucleolus-associated microRNAs. FEBS Open Bio. 4, 441-449. https://doi.org/10.1016/j.fob.2014.04.010 PMid:24918059 PMCid:PMC4050192
28. Bai, B., Yegnasubramanian, S., Wheelan, S. J., Laiho, M. (2014). RNA-Seq of the nucleolus reveals abundant SNORD44-derived small RNAs. PLoS One. 9(9):e107519. doi:10.1371/journal.pone.0107519. eCollection https://doi.org/10.1371/journal.pone.0107519
29. Probst, A. V., Okamoto, I., Casanova, M., El Marjou, F., Le Baccon, P., Almouzni, G. (2010). A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev. Cell. 19, 625-638. https://doi.org/10.1016/j.devcel.2010.09.002 PMid:20951352
30. Casanova, M., Pasternak, M., El Marjou, F., Le Baccon, P., Probst, A. V., Almouzni, G. (2013). Heterochromatin reorganization during early mouse development requires a single-stranded noncoding transcript. Cell Rep. 26, 1156-1167. https://doi.org/10.1016/j.celrep.2013.08.015 PMid:24055057
31. Santenard, A., Ziegler-Birling, C., Koch, M., Tora, L., Bannister, A. J., Torres-Padilla, M.E. (2010). Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol. 12, 853-862. https://doi.org/10.1038/ncb2089 PMid:20676102 PMCid:PMC3701880
32. Aguirre-Lavin, T., Adenot, P., Bonnet-Garnier, A., Lehmann, G., Fleurot, R., Boulesteix, C., Debey, P., Beaujean, N. (2012). 3D-FISH analysis of embryonic nuclei in mouse highlights several abrupt changes of nuclear organization during preimplantation development. BMC Dev. Biol. 12, 12-30. https://doi.org/10.1186/1471-213X-12-30 PMid:23095683 PMCid:PMC3517311
33. 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
34. Morovic, M., Strejcek, F., Fulka Jr., J., Hyttel, P., Laurincik, J. (2014). Proteomic disproportion of nucleoli in pig and mouse fully grown oocytes. European Biotechnology Congress 2014, J. Biotech., 185, Supplement, September 2014, Page 46. https://doi.org/10.1016/j.jbiotec.2014.07.155
35. Morovic, M., Strejcek, F., Nakagawa, S., Deshmukh, R. S., Murin, M., Benc, M., Fulka, H., Kyogoku, H., Pendovski, L., Fulka, J., Jr., Laurincik, J. (2017). Mouse oocytes nucleoli rescue embryonic development of porcine enucleolated oocytes, Zygote ahead of print.
36. Suh, N., Baehner, L., Moltzahn, F., Melton, C., Shenoy, A., Chen, J., Blelloch, R. (2010). MicroRNA function is globally suppressed in mouse oocytes and early embryos. Current Biol. 20, 271-277. https://doi.org/10.1016/j.cub.2009.12.044 PMid:20116247 PMCid:PMC2872512
37. Li, M., Xia, Y., Gu, Y., Zhang, K., Lang, Q., Chen, L., Guan, J., Luo, Z., Chen, H., Li, Y., Li, Q., Li, X., Jian, A., Shuai, S., Wang, J., Zhu, Q., Zhou, X., Gao, X., Li, X. (2010). MicroRNAome of porcine pre-and postnatal development. PLOS one 5:e11541. https://doi.org/10.1371/journal.pone.0011541 PMid:20634961 PMCid:PMC2902522
38. Niemann, H., Tina, X. C, King, E. A., Lee, R. S. F. (2008). Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction 135, 151-163. https://doi.org/10.1530/REP-07-0397 PMid:18239046
39. Benc, M., Strejcek, F., Murin, M., Morovic, M., Martinkova, S., Jettmarova, D., Pendovski, L., Fulka, J. Jr., Laurincik, J. (2017). Nucleologenesis and nucleolotransfer in mammalian oocytes:A review. Mac Vet Rev. 40 (2):117-124. https://doi.org/10.1515/macvetrev-2017-0023


Copyright 

©2018 Benc M. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Acknowledgement

This work was supported by Slovak Research and Development Agency under the contract No. APVV-14-0001, and also by the projects CZ.02.1.01/0.0/0.0/15_003/0000460, VEGA 1/0022/15, VEGA 1/0327/16 and Research Center AgroBioTech built in accordance with the project Building Research Centre „AgroBioTech” ITMS 26220220180. JF Jr. is supported from GACR 17-08605S.

Conflict of Interest Statement

The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 41, Issue 2, Pages 115-122, p-ISSN 1409-7621, e-ISSN 1857-7415, DOI: 10.2478/macvetrev-2018-0013, 2018