Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Localisation of RNAs and proteins in nucleolar precursor bodies of early mouse embryos

Elena Lavrentyeva A B , Kseniya Shishova A , German Kagarlitsky A and Olga Zatsepina A C
+ Author Affiliations
- Author Affiliations

A Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya Street, 16/10, Moscow, 117997, Russian Federation.

B Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, GSP-1, Leninskiye Gory, MSU, 1-73, Moscow, 119991, Russian Federation.

C Corresponding author. Email: zatsepina_olga@mail.ru

Reproduction, Fertility and Development 29(3) 509-520 https://doi.org/10.1071/RD15200

Abstract

Early embryos of all mammalian species contain morphologically distinct but transcriptionally silent nucleoli called the nucleolar precursor bodies (NPBs), which, unlike normal nucleoli, have been poorly studied at the biochemical level. To bridge this gap, here we examined the occurrence of RNA and proteins in early mouse embryos with two fluorochromes – an RNA-binding dye pyronin Y (PY) and the protein-binding dye fluorescein-5′-isothiocyanate (FITC). The staining patterns of zygotic NPBs were then compared with those of nucleolus-like bodies (NLBs) in fully grown surrounded nucleolus (SN)-type oocytes, which are morphologically similar to NPBs. We show that both entities contain proteins, but unlike NLBs, NPBs are significantly impoverished for RNA. Detectable amounts of RNA appear on the NPB surface only after resumption of rDNA transcription and includes pre-rRNAs and 28S rRNA as evidenced by fluorescence in situ hybridisation with specific oligonucleotide probes. Immunocytochemical assays demonstrate that zygotic NPBs contain rRNA processing factors fibrillarin, nucleophosmin and nucleolin, while UBF (the RNA polymerase I transcription factor) and ribosomal proteins RPL26 and RPS10 are not detectable. Based on the results obtained and data in the contemporary literature, we suggest a scheme of NPB assembly and maturation to normal nucleoli that assumes utilisation of maternally derived nucleolar proteins but of nascent rRNAs.

Additional keywords: confocal laser-scanning microscopy, early mammalian development, FITC, fluorescence in situ hybridisation, immunofluorescence, NPBs, nucleolar proteins, nucleolus-like bodies (NLBs), pyronin Y, rRNA.


References

Bachvarova, R., De Leon, V., Johnson, A., Kaplan, G., and Paynton, B. V. (1985). Changes in total RNA, polyadenylated RNA and actin mRNA during meiotic maturation of mouse oocytes. Dev. Biol. 108, 325–331.
Changes in total RNA, polyadenylated RNA and actin mRNA during meiotic maturation of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhsVKrsbg%3D&md5=a0c0dcc91c2980c1bb4818de24479a0eCAS | 2416609PubMed |

Baran, V., Veselá, J., Rehák, P., Koppel, J., and Fléchon, J. E. (1995). Localisation of fibrillarin and nucleolin in nucleoli of mouse preimplantation embryos. Mol. Reprod. Dev. 40, 305–310.
Localisation of fibrillarin and nucleolin in nucleoli of mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkt1Khs70%3D&md5=a80fac2a89c9726057fca7c5c1892025CAS | 7772340PubMed |

Biggiogera, M., Martin, T. E., Gordon, J., Amalric, F., and Fakan, S. (1994). Physiologically inactive nucleoli contain nucleoplasmic ribonucleoproteins: immunoelectron microscopy of mouse spermatids and early embryos. Exp. Cell Res. 213, 55–63.
Physiologically inactive nucleoli contain nucleoplasmic ribonucleoproteins: immunoelectron microscopy of mouse spermatids and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksl2htbc%3D&md5=f8505644afefb71dabbe67eef09bdaf7CAS | 8020606PubMed |

Bjerregaard, B., Wrenzycki, C., Strejcek, F., Laurincik, J., Holm, P., Ochs, R. L., Rosenkranz, C., Callesen, H., Rath, D., Niemann, H., and Maddox-Hyttel, P. (2004). Expression of nucleolar-related proteins in porcine preimplantation embryos produced in vivo and in vitro. Biol. Reprod. 70, 867–876.
Expression of nucleolar-related proteins in porcine preimplantation embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1Sitb4%3D&md5=6c912a890a678c4a326d7d5a0b6aee1eCAS | 14585813PubMed |

Bogolyubova, I. O. (2011). Transcriptional activity of nuclei in two-cell blocked mouse embryos. Tissue Cell 43, 262–265.
Transcriptional activity of nuclei in two-cell blocked mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1yhurg%3D&md5=658b064bca9b631c0fac9db76310985bCAS | 21511319PubMed |

Boisvert, F.-M., Van Koningsbruggen, S., Navascués, J., and Lamond, A. I. (2007). The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8, 574–585.
| 1:CAS:528:DC%2BD2sXmvVaktLo%3D&md5=da7a4eeb0e010fa1bf40699c58a3ad5dCAS | 17519961PubMed |

Bonnet-Garnier, A., Feuerstein, P., Chebrout, M., Fleurot, R., Jan, H. U., Debey, P., and Beaujean, N. (2012). Genome organisation and epigenetic marks in mouse germinal vesicle oocytes. Int. J. Dev. Biol. 56, 877–887.
Genome organisation and epigenetic marks in mouse germinal vesicle oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVyqsLc%3D&md5=52f97623f2c15a7a3baa6a23116089f0CAS | 23417410PubMed |

Bouniol, C., Nguyen, E., and Debey, P. (1995). Endogenous transcription occurs at the one-cell stage in the mouse embryo. Exp. Cell Res. 218, 57–62.
Endogenous transcription occurs at the one-cell stage in the mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsFShsLc%3D&md5=1135b6529d6f6c0934266d22814715c5CAS | 7537698PubMed |

Braude, P., Bolton, V., and Moore, S. (1988). Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332, 459–461.
Human gene expression first occurs between the four- and eight-cell stages of preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVCiurk%3D&md5=9d44f9bc2c29bf54c058e52680a95489CAS | 3352746PubMed |

Darzynkiewicz, Z., Kapuscinski, J., Traganos, F., and Crissman, H. A. (1987). Application of pyronin Y(G) in cytochemistry of nucleic acids. Cytometry 8, 138–145.
Application of pyronin Y(G) in cytochemistry of nucleic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktVemt74%3D&md5=c538360aebc0f62614b3bb5c458172fbCAS | 2438101PubMed |

Duncan, F. E., and Schultz, R. M. (2010). Gene expression profiling of mouse oocytes and preimplantation embryos. Methods Enzymol. 477, 457–480.
Gene expression profiling of mouse oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Ols7rO&md5=97b5101ce1e8c148e2ca576d8ea0fe78CAS | 20699155PubMed |

Engel, W., Zenzes, M. T., and Schmid, M. (1977). Activation of mouse ribosomal RNA genes at the two-cell stage. Hum. Genet. 38, 57–63.
Activation of mouse ribosomal RNA genes at the two-cell stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXlvVWmt74%3D&md5=d39d01442a5a1c71d810d9332baf4aaeCAS | 903155PubMed |

Fakan, S., and Odartchenko, N. (1980). Ultrastructural organisation of the cell nucleus in early mouse embryos. Biol. Cell. 37, 211–218.

Farley, K. I., Surovtseva, Y., Merkel, J., and Baserga, S. J. (2015). Determinants of mammalian nucleolar architecture. Chromosoma , .
Determinants of mammalian nucleolar architecture.Crossref | GoogleScholarGoogle Scholar | 25670395PubMed |

Ferreira, J., and Carmo-Fonseca, M. (1995). The biogenesis of the coiled body during early mouse development. Development 121, 601–612.
| 1:CAS:528:DyaK2MXjsl2ntLc%3D&md5=ebf5db8b6eb37fb1e23a962ac7ead5f8CAS | 7768196PubMed |

Fléchon, J. E., and Kopecný, 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.
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.Crossref | GoogleScholarGoogle Scholar | 9770784PubMed |

Fulka, H., and Fulka, J. (2010). Nucleolar transplantation in oocytes and zygotes: challenges for further research. Mol. Hum. Reprod. 16, 63–67.
Nucleolar transplantation in oocytes and zygotes: challenges for further research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlCitQ%3D%3D&md5=be8a19aa255ce054f07aff0c06eb5526CAS | 19819895PubMed |

Fulka, H., and Langerova, A. (2014). The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte-to-embryo transition. Development 141, 1694–1704.
The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte-to-embryo transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslOmu7g%3D&md5=37de2e91f1b63a2db5bfef6d8db6b784CAS | 24715459PubMed |

Geuskens, M., and Alexandre, H. (1984). Ultrastructural and autoradiographic studies of nucleolar development and rDNA transcription in preimplantation mouse embryos. Cell Differ. 14, 125–134.
Ultrastructural and autoradiographic studies of nucleolar development and rDNA transcription in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlsVykur4%3D&md5=83bac87764dbf1e81bf03d3713da2778CAS | 6467377PubMed |

Graf, A., Krebs, S., Heininen-Brown, M., Zakhartchenko, V., Blum, H., and Wolf, E. (2014). Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments. Anim. Reprod. Sci. 149, 46–58.
Genome activation in bovine embryos: review of the literature and new insights from RNA sequencing experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVymu7bF&md5=15ee4fa5e714aef756805eaea687603aCAS | 24975847PubMed |

Hamatani, T., Ko, M. Sh., Yamada, M., Kuji, N., Mizusawa, Y., Shoji, M., Hada, T., Asada, H., Maruyama, T., and Yoshimura, Y. (2006). Global gene expression profiling of preimplantation embryos. Hum. Cell 19, 98–117.
Global gene expression profiling of preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 17204093PubMed |

Hernandez-Verdun, D. (2011). Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2, 189–194.
Assembly and disassembly of the nucleolus during the cell cycle.Crossref | GoogleScholarGoogle Scholar | 21818412PubMed |

Hyttel, P., Laurincik, J., Viuff, D., Fair, T., Zakhartchenko, V., Rosenkranz, C., Avery, B., Rath, D., Niemann, H., Thomsen, P. D., Schellander, K., Callesen, H., Wolf, E., Ochs, R. L., and Greve, T. (2000). Activation of ribosomal RNA genes in preimplantation cattle and swine embryos. Anim. Reprod. Sci. 60–61, 49–60.
Activation of ribosomal RNA genes in preimplantation cattle and swine embryos.Crossref | GoogleScholarGoogle Scholar | 10844184PubMed |

Ihara, M., Tseng, H., and Schultz, R. M. (2011). Expression of variant ribosomal RNA genes in mouse oocytes and preimplantation embryos. Biol. Reprod. 84, 944–946.
Expression of variant ribosomal RNA genes in mouse oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGisrs%3D&md5=41b33a84f9098a2c703d3fb2300a4c1bCAS | 21209414PubMed |

Kapuscinski, J., and Darzynkiewicz, Z. (1987). Interactions of pyronin Y(G) with nucleic acids. Cytometry 8, 129–137.
Interactions of pyronin Y(G) with nucleic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXitFSgsrw%3D&md5=35047038ccf52ae1823da43c3478834eCAS | 3582061PubMed |

Kopečný, V., Landa, V., and Pavlok, A. (1995). Localisation of nucleic acids in the nucleoli of oocytes and early embryos of mouse and hamster: an autoradiographic study. Mol. Reprod. Dev. 41, 449–458.
Localisation of nucleic acids in the nucleoli of oocytes and early embryos of mouse and hamster: an autoradiographic study.Crossref | GoogleScholarGoogle Scholar | 7576612PubMed |

Kyogoku, H., Kitajima, T. S., and Miyano, T. (2014a). Nucleolus precursor body (NPB): a distinct structure in mammalian oocytes and zygotes. Nucleus 5, 493–498.
Nucleolus precursor body (NPB): a distinct structure in mammalian oocytes and zygotes.Crossref | GoogleScholarGoogle Scholar | 25495074PubMed |

Kyogoku, H., Fulka, J., Wakayama, T., and Miyano, T. (2014b). De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes. Development 141, 2255–2259.
De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOht7jK&md5=52958c9788760c8b986e616feb2dab79CAS | 24803589PubMed |

Laurincik, J., Thomsen, P. D., Hay-Schmidt, A., Avery, B., Greve, T., Ochs, R. L., and Hyttel, P. (2000). Nucleolar proteins and nuclear ultrastructure in preimplantation bovine embryos produced in vitro. Biol. Reprod. 62, 1024–1032.
Nucleolar proteins and nuclear ultrastructure in preimplantation bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFajtb4%3D&md5=c779f6e7f9a2baf835a52bc6f17b04b7CAS | 10727273PubMed |

Laurincik, J., Schmoll, F., Mahabir, E., Schneider, H., Stojkovic, M., Zakhartchenko, V., Prelle, K., Hendrixen, P. J., Voss, P. L., Moeszlacher, G. G., Avery, B., Dieleman, S. J., Besenfelder, U., Müller, M., Ochs, R. L., Wolf, E., Schellander, K., and Maddox-Hyttel, P. (2003). Nucleolar proteins and ultrastructure in bovine in vivo-developed, in vitro-produced and parthenogenetic cleavage-stage embryos. Mol. Reprod. Dev. 65, 73–85.
Nucleolar proteins and ultrastructure in bovine in vivo-developed, in vitro-produced and parthenogenetic cleavage-stage embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXis1als7k%3D&md5=fb0b9f23a7006adf63f334454f2c86b6CAS | 12658636PubMed |

Lazdins, I. B., Delannoy, M., and Sollner-Webb, B. (1997). Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridisation. Chromosoma 105, 481–495.
Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVGntrk%3D&md5=2028fa86c155f9478e9a524a3c8a1368CAS | 9211976PubMed |

Li, J.-J., Lian, H.-Y., Zhang, S.-Y., Cui, W., Sui, H.-S., Han, D., and Liu, N. (2012). Regulation of fusion of the nucleolar precursor bodies following activation of mouse oocytes: roles of the maturation-promoting factors and mitogen-activated protein kinases. Zygote 20, 291–303.
Regulation of fusion of the nucleolar precursor bodies following activation of mouse oocytes: roles of the maturation-promoting factors and mitogen-activated protein kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVWjsrzL&md5=3596fc9038363c7a0240b79e21db7943CAS | 21554769PubMed |

Morris, S. A., and Zernicka-Goetz, M. (2012). Formation of distinct cell types in the mouse blastocyst. Results Probl. Cell Differ. 55, 203–217.
Formation of distinct cell types in the mouse blastocyst.Crossref | GoogleScholarGoogle Scholar | 22918808PubMed |

Mullineux, S. T., and Lafontaine, D. L. (2012). Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie 94, 1521–1532.
Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtV2rsrw%3D&md5=801e41558d67f5d8471de403da908d1aCAS | 22342225PubMed |

Oestrup, O., Hall, V., Petkov, S. G., Wolf, X. A., Hyldig, S., and Hyttel, P. (2009). From zygote to implantation: morphological and molecular dynamics during embryo development in the pig. Reprod. Domest. Anim. 44, 39–49.
From zygote to implantation: morphological and molecular dynamics during embryo development in the pig.Crossref | GoogleScholarGoogle Scholar | 19660079PubMed |

Ogushi, S., and Saitou, M. (2010). The nucleolus in the mouse oocyte is required for the early step of both female and male pronucleus organisation. J. Reprod. Dev. 56, 495–501.
The nucleolus in the mouse oocyte is required for the early step of both female and male pronucleus organisation.Crossref | GoogleScholarGoogle Scholar | 20519829PubMed |

Ogushi, S., Palmieri, C., Fulka, H., Saitou, M., Miyano, T., and Fulka, J. (2008). The maternal nucleolus is essential for early embryonic development in mammals. Science 319, 613–616.
The maternal nucleolus is essential for early embryonic development in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Knt7w%3D&md5=a6de54dfeec850d72c5c7b102f3da90dCAS | 18239124PubMed |

Papale, L., Fiorentino, A., Montag, M., and Tomasi, G. (2012). The zygote. Hum. Reprod. 27, i22–i49.
The zygote.Crossref | GoogleScholarGoogle Scholar | 22811310PubMed |

Paynton, B. V., Rempel, R., and Bachvarova, R. (1988). Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. Dev. Biol. 129, 304–314.
Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXls1Oqs74%3D&md5=d4e6de29be668af84dabc3d7cc93cd5aCAS | 2458285PubMed |

Rodriguez-Zas, S. L., Schellander, K., and Lewin, H. A. (2008). Biological interpretations of transcriptomic profiles in mammalian oocytes and embryos. Reproduction 135, 129–139.
Biological interpretations of transcriptomic profiles in mammalian oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1yrt7k%3D&md5=e4347d1269623631a4b7b053243412adCAS | 18239044PubMed |

Romanova, L. G., Anger, M., Zatsepina, O. V., and Schultz, R. M. (2006a). Implication of nucleolar protein SURF6 in ribosome biogenesis and preimplantation mouse development. Biol. Reprod. 75, 690–696.
Implication of nucleolar protein SURF6 in ribosome biogenesis and preimplantation mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgt7jK&md5=4c4dbfc43dd3f934bec6ab6b8ca9e783CAS | 16855206PubMed |

Romanova, L., Korobova, F., Noniashvilli, E., Dyban, A., and Zatsepina, O. (2006b). High-resolution mapping of ribosomal DNA in early mouse embryos by fluorescence in situ hybridisation. Biol. Reprod. 74, 807–815.
High-resolution mapping of ribosomal DNA in early mouse embryos by fluorescence in situ hybridisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjsl2jtbw%3D&md5=382d83ad5bc42ce70a1cde3cc6870ac1CAS | 16421232PubMed |

Schultz, R. M. (2002). The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. 8, 323–331.
The molecular foundations of the maternal to zygotic transition in the preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVOgtLY%3D&md5=c1ca6002c9cebbf58d97b10a50ea880bCAS |

Shishova, K. V., Lavrentyeva, E. A., Dobrucki, J. W., and 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.
Nucleolus-like bodies of fully grown mouse oocytes contain key nucleolar proteins but are impoverished for rRNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVyhu77I&md5=7d3708ffaf5065a7e9bed4f9daa398ebCAS | 25481757PubMed |

Svarcova, O., Dinnyes, A., Polgar, Z., Bodo, S., Adorjan, M., Meng, Q., and Maddox-Hyttel, P. (2009). Nucleolar re-activation is delayed in mouse embryos cloned from two different cell lines. Mol. Reprod. Dev. 76, 132–141.
Nucleolar re-activation is delayed in mouse embryos cloned from two different cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1SjsQ%3D%3D&md5=4802fedcd5e16042bd418c46d3ad9c25CAS | 18470874PubMed |

Tesarík, J., Kopecný, V., Plachot, M., and Mandelbaum, J. (1987). High-resolution autoradiographic localisation of DNA-containing sites and RNA synthesis in developing nucleoli of human preimplantation embryos: a new concept of embryonic nucleogenesis. Development 101, 777–791.
| 2460303PubMed |

Vogt, E. J., Meglicki, M., Hartung, K. I., Borsuk, E., and Behr, R. (2012). Importance of the pluripotency factor LIN28 in the mammalian nucleolus during early embryonic development. Development 139, 4514–4523.
Importance of the pluripotency factor LIN28 in the mammalian nucleolus during early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Ohtrg%3D&md5=eb6e734cbcf3ef77968e36ea30bb5f1aCAS | 23172912PubMed |

Wang, Q. T., Piotrowska, K., Ciemerych, M. A., Milenkovic, L., Scott, M. P., Davis, R. W., and Zernicka-Goetz, M. (2004). A genome-wide study of gene activity reveals developmental signalling pathways in the preimplantation mouse embryo. Dev. Cell 6, 133–144.
A genome-wide study of gene activity reveals developmental signalling pathways in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlaktQ%3D%3D&md5=21a7d6e865e70f598316f67c871df4aaCAS | 14723853PubMed |

Zatsepina, O. V., Voit, R., Grummt, I., Spring, H., Semenov, M. V., and Trendelenburg, M. F. (1993). The RNA polymerase I-specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes. Chromosoma 102, 599–611.
The RNA polymerase I-specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFers7o%3D&md5=c0b4c2875d039352f224c623cd55db92CAS | 8306821PubMed |

Zatsepina, O. V., Bouniol-Baly, C., Amirand, C., and Debey, P. (2000). Functional and molecular reorganisation of the nucleolar apparatus in maturing mouse oocytes. Dev. Biol. 223, 354–370.
Functional and molecular reorganisation of the nucleolar apparatus in maturing mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFeqs7w%3D&md5=3dd0896bea540a11e2ca5bc337ac876eCAS | 10882521PubMed |

Zatsepina, O., Baly, C., Chebrout, M., and 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.
The step-wise assembly of a functional nucleolus in preimplantation mouse embryos involves the Cajal (coiled) body.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFyisLw%3D&md5=f318cdee706856baaba16c589e3b7b11CAS | 12490198PubMed |

Zeng, F., and Schultz, R. M. (2005). RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev. Biol. 283, 40–57.
RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGitL8%3D&md5=b21f475c6e93e427298e562b4daa0219CAS | 15975430PubMed |

Zhang, K., Huang, K., Luo, Y., and Li, S. (2014). Identification and functional analysis of long non-coding RNAs in mouse cleavage stage embryonic development based on single-cell transcriptome data. BMC Genomics 15, 845.
Identification and functional analysis of long non-coding RNAs in mouse cleavage stage embryonic development based on single-cell transcriptome data.Crossref | GoogleScholarGoogle Scholar | 25277336PubMed |