Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-28T17:41:53.849Z Has data issue: false hasContentIssue false
  • English
  • Français

Mouse oocytes nucleoli rescue embryonic development of porcine enucleolated oocytes

Published online by Cambridge University Press:  20 November 2017

Martin Morovic ,
Frantisek Strejcek ,
Shoma Nakagawa ,
Rahul S. Deshmukh ,
Matej Murin ,
Michal Benc ,
Helena Fulka ,
Hirohisa Kyogoku ,
Lazo Pendovski  and
Josef Fulka Jr
...Show all authors
Martin Morovic*
Affiliation:
Department of Zoology and Anthropology, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Nabrezie mladeze 91, 949 74, Nitra, Slovakia.
Frantisek Strejcek
Affiliation:
Constantine the Philosopher University, Nitra, Slovak Republic.
Shoma Nakagawa
Affiliation:
Institute of Animal Science, Prague, Czech Republic. Centre de Recherche du Centre Hospitalier du l'Université de Montreal (CRCHUM), Quebec, Canada.
Rahul S. Deshmukh
Affiliation:
Bombay Veterinary College, Mumbai, India.
Matej Murin
Affiliation:
Constantine the Philosopher University, Nitra, Slovak Republic.
Michal Benc
Affiliation:
Constantine the Philosopher University, Nitra, Slovak Republic. Institute of Animal Science, Prague, Czech Republic.
Helena Fulka
Affiliation:
Institute of Animal Science, Prague, Czech Republic. Institute of Molecular Genetics of the ASCR, Prague, Czech Republic.
Hirohisa Kyogoku
Affiliation:
RIKEN Kobe, Kobe, Japan.
Lazo Pendovski
Affiliation:
Ss. Cyril and Methodius University in Skopje, Republic of Macedonia.
Josef Fulka Jr
Affiliation:
Institute of Animal Science, Prague, Czech Republic.
Jozef Laurincik
Affiliation:
Constantine the Philosopher University, Nitra, Slovak Republic. Institute of Animal Physiology and Genetics ASCR, Libechov, Czech Republic. Catholic University, Ruzomberok, Slovakia.
*
All correspondence to: Martin Morovic. Department of Zoology and Anthropology, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Nabrezie mladeze 91, 949 74, Nitra, Slovakia. Tel: +421 37 6408 712. Fax: +421 37 6408 556. E-mail: mmorovic@ukf.sk
Get access Rights & Permissions [Opens in a new window]

Summary

It is well known that nucleoli of fully grown mammalian oocytes are indispensable for embryonic development. Therefore, the embryos originated from previously enucleolated (ENL) oocytes undergo only one or two cleavages and then their development ceases. In our study the interspecies (mouse/pig) nucleolus transferred embryos (NuTE) were produced and their embryonic development was analyzed by autoradiography, transmission electron microscopy (TEM) and immunofluorescence (C23 and upstream binding factor (UBF)). Our results show that the re-injection of isolated oocyte nucleoli, either from the pig (P + P) or mouse (P + M), into previously enucleolated and subsequently matured porcine oocytes rescues their development after parthenogenetic activation and some of these develop up to the blastocyst stage (P + P, 11.8%; P + M, 13.5%). In nucleolus re-injected 8-cell and blastocyst stage embryos the number of nucleoli labeled with C23 in P + P and P + M groups was lower than in control (non-manipulated) group. UBF was localized in small foci within the nucleoli of blastocysts in control and P + P embryos, however, in P + M embryos the labeling was evenly distributed in the nucleoplasm. The TEM and autoradiographic evaluations showed the formation of functional nucleoli and de novo rRNA synthesis at the 8-cell stage in both, control and P + P group. In the P + M group the formation of comparable nucleoli was delayed. In conclusion, our results indicate that the mouse nucleolus can rescue embryonic development of enucleolated porcine oocytes, but the localization of selected nucleolar proteins, the timing of transcription activation and the formation of the functional nucleoli in NuTE compared with control group show evident aberrations.

Keywords

EmbryoInterspecies nucleolar transferMouseNucleolusOocytesPig
Type
Research Article
Information
Zygote , Volume 25 , Issue 6 , December 2017 , pp. 675 - 685
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmed, K., Dehghani, H., Rugg-Gunn, P., Fussner, E., Rossant, J. & Bazett-Jones, D.P. (2010). Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS One 5, e10531.CrossRefGoogle ScholarPubMed
Antoine, N., Lepoint, A., Baeckeland, E. & Goessens, G. (1987). Evolution of the rat oocyte nucleolus during follicular growth. Biol. Cell 59, 107–12.CrossRefGoogle ScholarPubMed
Barnetova, I., Morovic, M., Strejcek, F., Østrup, O., Hyttel, P., Niemann, H., Laurincik, J., Fulka, J. & Fulka, H. (2012). RNA polymerase II transcriptional silencing in growing and fully grown germinal vesicle oocytes isolated from gonadotropin-stimulated and non-stimulated gilts. Mol. Reprod. Dev. 79, 697–708.CrossRefGoogle ScholarPubMed
Bjerregaard, B., Wrenzycki, C., Strejcek, F., Laurincik, J., Holm, P., Ochs, R. L., Rosenkranz, Ch., 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, 867–76.CrossRefGoogle ScholarPubMed
Chen, D. & Huang, S. (2001). Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J. Cell Biol. 153, 169–76.CrossRefGoogle ScholarPubMed
Deshmukh, R. S., Østrup, O., Strejcek, F., Vejlsted, M., Lucas-Hahn, A., Petersen, B., Li, J., Callesen, H., Niemann, H. & Hyttel, P. (2012). Early aberrations in chromatin dynamics in embryos produced under in vitro conditions. Cell. Reprogram. 14, 225–34.CrossRefGoogle ScholarPubMed
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, 183–91.CrossRefGoogle ScholarPubMed
Fulka, H. & Aoki, F. (2016). Nucleolus precursor bodies and ribosome biogenesis in early mammalian embryos: Old theories and new discoveries. Biol. Reprod. 94, 143–1.CrossRefGoogle ScholarPubMed
Fulka, H. & Fulka, J. (2010). Nucleolar transplantation in oocytes and zygotes: challenges for further research. Mol. Hum. Reprod. 16, 63–7.CrossRefGoogle ScholarPubMed
Fulka, H. & Langerova, A. (2014). The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition. Development 141, 1694–704.CrossRefGoogle Scholar
Fulka, J. Jr, Moor, R.M., Loi, P. & Fulka, J. (2003). Enucleolation of porcine oocytes. Theriogenology 59, 1879–85.CrossRefGoogle ScholarPubMed
Gavrilova, E. V., Kuznetsova, I.S., Enukashvily, N.I., Noniashvili, E.M., Dyban, A.P. & Podgornaya, O.I. (2009). Localization of satellite DNA and associated proteins in respect to nucleolar precursor bodies in one-and two-cell mouse embryos. Cell Tissue Biol. 3, 213–21.CrossRefGoogle Scholar
Hyttel, P. & Madsen, I. (1987). Rapid method to prepare mammalian oocytes and embryos for transmission electron microscopy. Cells Tissues Organs 129, 12–4.CrossRefGoogle ScholarPubMed
Hyttel, P., Laurincik, J., Rosenkranz, C., Rath, D., Niemann, H., Ochs, R. L., & Schellander, K. (2000). Nucleolar proteins and ultrastructure in preimplantation porcine embryos developed in vivo . Biol. Reprod. 63, 1848–56.CrossRefGoogle ScholarPubMed
Hyttel, P., Viuff, D., Fair, T., Laurincik, J., Thomsen, P. D., Callesen, H., Vos, P. L., Hendriksen, P. J., Dieleman, S. J., Schellander, K., Besenfelder, U. & Greve, T. (2001). Ribosomal RNA gene expression and chromosome aberrations in bovine oocytes and preimplantation embryos. Reproduction 122, 21–30.CrossRefGoogle ScholarPubMed
King, W.A., Niar, A., Chartrain, I., Betteridge, K.J. & Guay, P. (1988). Nucleolus organizer regions and nucleoli in preattachment bovine embryos. J. Reprod. Fertil. 82, 87–95.CrossRefGoogle ScholarPubMed
Kopecny, V., Biggiogera, M., Laurincik, J., Pivko, J., Grafenau, P., Martin, T.E., 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, 561–74.CrossRefGoogle ScholarPubMed
Kyogoku, H., Kitajima, T.S., & Miyano, T. (2014). Nucleolus precursor body (NPB): a distinct structure in mammalian oocytes and zygotes. Nucleus 5, 493–8.CrossRefGoogle ScholarPubMed
Lagutina, I., Fulka, H., Brevini, T.A., Antonini, S., Brunetti, D., Colleoni, S., Gandolfi, F., Lazzari, G., Fulka, J. Jr & Galli, C. (2010). Development, embryonic genome activity and mitochondrial characteristics of bovine-pig inter-family nuclear transfer embryos. Reproduction 140, 273–85.CrossRefGoogle ScholarPubMed
Lagutina, I., Zakhartchenko, V., Fulka, H., Colleoni, S., Wolf, E., Fulka, J. Jr, Lazzari, J. & Galli, C. (2011). Formation of nucleoli in interspecies nuclear transfer embryos derived from bovine, porcine, and rabbit oocytes and nuclear donor cells of various species. Reproduction 141, 453–65.CrossRefGoogle ScholarPubMed
Laurincik, J., Bjerregaard, B., Strejcek, F., Rath, D., Niemann, H., Rosenkranz, C., Ochs, R.L. & Maddox-Hyttel, P. (2004). Nucleolar ultrastructure and protein allocation in in vitro produced porcine embryos. Mol. Reprod. Dev. 68, 327–34.CrossRefGoogle ScholarPubMed
Laurincik, J., Thomsen, P.D., Hay-Schmidt, A., Avery, B., Greve, T., Ochs, R.L. & Hyttel, P. (2000). Nucleolar proteins and nuclear ultrastructure in preimplantation bovine embryos produced in vitro . Biol. Reprod. 62, 1024–32.CrossRefGoogle ScholarPubMed
Lefevre, B. (2008). The nucleolus of the maternal gamete is essential for life. BioEssays 30, 613–6.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Martin, C., Beaujean, N., Brochard, V., Audouard, C., Zink, D. & Debey, P. (2006). Genome restructuring in mouse embryos during reprogramming and early development. Dev. Biol. 292, 317–32.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 613–6.CrossRefGoogle ScholarPubMed
Østrup, O., Hall, V., Petkov, S.G., Wolf, X. A., Hyldig, S. & Hyttel, P. (2009). From zygote to implantation: morphological and molecular dynamics during embryo development in the pig. Reprod. Domest. Anim. 44, 39–49.CrossRefGoogle Scholar
Østrup, O., Strejcek, F., Petrovicova, I., Lucas-Hahn, A., Morovic, M., Lemme, E., Petersen, B., Laurincikova, N., Niemann, H., Laurincik, J. & Hyttel, P. (2011). Role of ooplasm in nuclear and nucleolar remodeling of intergeneric somatic cell nuclear transfer embryos during the first cell cycle. Cell. Reprogram. 13, 145–55.CrossRefGoogle ScholarPubMed
Pichugin, A., Le Bourhis, D., Adenot, P., Lehmann, G., Audouard, C., Renard, J.P., Vignon, X. & Beaujean, N. (2010). Dynamics of constitutive heterochromatin: two contrasted kinetics of genome restructuring in early cloned bovine embryos. Reproduction 139, 129–37.CrossRefGoogle ScholarPubMed
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, 267–81.CrossRefGoogle ScholarPubMed
Song, B.S., Lee, S.H., Kim, S.U., Kim, J.S., Park, J.S., Kim, C.H., Chang, K.T., Han, Y.M., Lee, K.K., Lee, D.S. & Koo, D.B. (2009). Nucleologenesis and embryonic genome activation are defective in interspecies cloned embryos between bovine ooplasm and rhesus monkey somatic cells. BMC Dev. Biol. 9, 44.CrossRefGoogle ScholarPubMed
Tesarik, J., Travnik, P., Kopecny, V. & Kristek, F. (1983). Nucleolar transformations in the human oocyte after completion of growth. Gamete Res. 8, 267–77.CrossRefGoogle Scholar
Tomanek, M., Kopecny, V. & Kanka, J. (1989). Genome reactivation in developing early pig embryos: an ultrastructural and autoradiographic analysis. Anat. Embryol. 180, 309–16.CrossRefGoogle ScholarPubMed