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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Temporal and spatial control of gene expression in early embryos of farm animals

Tiziana A. L. Brevini A B , Fabiana Cillo A , Stefania Antonini A , Valentina Tosetti A and Fulvio Gandolfi A
+ Author Affiliations
- Author Affiliations

A Department of Anatomy of Domestic Animals, School of Veterinary Medicine, University of Milan, Italy.

B Corresponding author. Email: tiziana.brevini@unimi.it

Reproduction, Fertility and Development 19(1) 35-42 https://doi.org/10.1071/RD06119
Published: 12 December 2006

Abstract

A gradual transition from oocyte-derived mRNA and proteins to full embryonic transcription characterises early embryonic development. Messenger RNAs and proteins of maternal origin are accumulated into the oocyte throughout its growth in the ovary. Upon fertilisation, several mechanisms are activated that control the appropriate use of such material and prepare for the synthesis of new products. The present review will describe some of the mechanisms active in early embryos of domestic species. Data will be presented on the control of gene expression by the 3′ untranslated regions and their interaction with specialised sequences at the 5′ cap end. The process of RNA sorting and localisation, initially described in different cell types and in oocytes of lower species, will also be discussed, particularly in relation to its possible role in regulating early pig development. Finally, specific genes involved in the activation of cattle embryonic transcription will be described. This brief overview will provide some suggestions on how these different mechanisms may be integrated and cooperate to ensure the correct initiation of embryonic development.

Extra keywords: cytoplasmic streaming, maternal–embryonic transition, mRNA polyadenylation, staufen, zygote arrest 1 (Zar1).


References

Aoki, F. , Worrad, D. M. , and Schultz, R. M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296–307.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Barnes, F. L. , and First, N. L. (1991). Embryonic transcription in in vitro cultured bovine embryos. Mol. Reprod. Dev. 29, 117–123.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Bateman, M. J. , Cornell, R. , d'Alencon, C. , and Sandra, A. (2004). Expression of the zebrafish Staufen gene in the embryo and adult. Gene Expr. Patterns 5, 273–278.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Brevini, T. A. , Lonergan, P. , Cillo, F. , Francisci, C. , Favetta, L. A. , Fair, T. , and Gandolfi, F. (2002). Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol. Reprod. Dev. 63, 510–517.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Brevini, T. A. , Cillo, F. , Colleoni, S. , Lazzari, G. , Galli, C. , and Gandolfi, F. (2004). Expression pattern of the maternal factor zygote arrest 1 (Zar1) in bovine tissues, oocytes, and embryos. Mol. Reprod. Dev. 69, 375–380.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Brevini, T. A. L. , Cillo, F. , Antonini, S. , and Gandolfi, F. (2006). Cytoplasmic remodeling and the acquisition of developmental competence in pig oocytes. Anim. Reprod. Sci., ,in press.


Brevini Gandolfi, T. A. L. , and Gandolfi, F. (2001). The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–1276.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Brevini-Gandolfi, T. A. , Favetta, L. A. , Mauri, L. , Luciano, A. M. , Cillo, F. , and Gandolfi, F. (1999). Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol. Reprod. Dev. 52, 427–433.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Broadus, J. , Fuerstenberg, S. , and Doe, C. Q. (1998). Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391, 792–795.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Christians, E. , Davis, A. A. , Thomas, S. D. , and Benjamin, I. J. (2000). Maternal effect of Hsf1 on reproductive success. Nature 407, 693–694.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Cohen, R. S. (2002). Oocyte patterning: dynein and kinesin, inc. Curr. Biol. 12, R797–R799.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Combelles, C. M. , and Albertini, D. F. (2001). Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev. Biol. 239, 281–294.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Dai, Y. , Newman, B. , and Moor, R. (2005). Translational regulation of MOS messenger RNA in pig oocytes. Biol. Reprod. 73, 997–1003.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Dalbies-Tran, R. , Papillier, P. , Pennetier, S. , Uzbekova, S. , and Monget, P. (2005). Bovine mater-like NALP9 is an oocyte marker gene. Mol. Reprod. Dev. 71, 414–421.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gavis, E. R. , and Lehmann, R. (1992). Localization of nanos RNA controls embryonic polarity. Cell 71, 301–313.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Groisman, I. , Jung, M. Y. , Sarkissian, M. , Cao, Q. , and Richter, J. D. (2002). Translational control of the embryonic cell cycle. Cell 109, 473–483.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gurdon, J. B. (1992). The generation of diversity and pattern in animal development. Cell 68, 185–199.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hachet, O. , and Ephrussi, A. (2004). Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428, 959–963.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hake, L. E. , and Richter, J. D. (1997). Translational regulation of maternal mRNA. Biochim. Biophys. Acta 1332, M31–M38.
PubMed |

Hamatani, T. , Carter, M. G. , Sharov, A. A. , and Ko, M. S. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117–131.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Huang, Y. S. , and Richter, J. D. (2004). Regulation of local mRNA translation. Curr. Opin. Cell Biol. 16, 308–313.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Jansen, R. P. (1999). RNA–cytoskeletal associations. FASEB J. 13, 455–466.
PubMed |

King, M. L. , Zhou, Y. , and Bubunenko, M. (1999). Polarizing genetic information in the egg: RNA localization in the frog oocyte. Bioessays 21, 546–557.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lasko, P. (1999). RNA sorting in Drosophila oocytes and embryos. FASEB J. 13, 421–433.
PubMed |

Latham, K. E. (1999). Mechanisms and control of embryonic genome activation in mammalian embryos. Int. Rev. Cytol. 193, 71–124.
PubMed |

Maddox-Hyttel, P. , Bjerregaard, B. , and Laurincik, J. (2005). Meiosis and embryo technology: renaissance of the nucleolus. Reprod. Fertil. Dev. 17, 3–14.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Martin, K. C. , Casadio, A. , Zhu, H. , Yaping, E. , Rose, J. C. , Chen, M. , Bailey, C. H. , and Kandel, E. R. (1997). Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927–938.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Niessing, D. , Blanke, S. , and Jackle, H. (2002). Bicoid associates with the 5′-cap-bound complex of caudal mRNA and represses translation. Genes Dev. 16, 2576–2582.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ostermeier, G. C. , Miller, D. , Huntriss, J. D. , Diamond, M. P. , and Krawetz, S. A. (2004). Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429, 154.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Paris, J. , and Richter, J. D. (1990). Maturation-specific polyadenylation and translational control: diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes. Mol. Cell. Biol. 10, 5634–5645.
PubMed |

Paris, J. , Swenson, K. , Piwnica-Worms, H. , and Richter, J. D. (1991). Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. Genes Dev. 5, 1697–1708.
PubMed |

Pennetier, S. , Uzbekova, S. , Perreau, C. , Papillier, P. , Mermillod, P. , and Dalbies-Tran, R. (2004). Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos. Biol. Reprod. 71, 1359–1366.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pennetier, S. , Perreau, C. , Uzbekova, S. , Thelie, A. , Delaleu, B. , Mermillod, P. , and Dalbies-Tran, R. (2006). MATER protein expression and intracellular localization throughout bovine folliculogenesis and preimplantation embryo development. BMC Dev. Biol. 6, 26.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pocar, P. , Brevini, T. A. , Perazzoli, F. , Cillo, F. , Modina, S. , and Gandolfi, F. (2001). Cellular and molecular mechanisms mediating the effects of polychlorinated biphenyls on oocyte developmental competence in cattle. Mol. Reprod. Dev. 60, 535–541.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pocar, P. , Brevini, T. A. , Fischer, B. , and Gandolfi, F. (2003). The impact of endocrine disruptors on oocyte competence. Reproduction 125, 313–325.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Proudfoot, N. (2000). Connecting transcription to messenger RNA processing. Trends Biochem. Sci. 25, 290–293.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Richter, J. D. , and Sonenberg, N. (2005). Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433, 477–480.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shatkin, A. J. , and Manley, J. L. (2000). The ends of the affair: capping and polyadenylation. Nat. Struct. Biol. 7, 838–842.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shav-Tal, Y. , and Singer, R. H. (2005). RNA localization. J. Cell Sci. 118, 4077–4081.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Song, J. L. , and Wessel, G. M. (2005). How to make an egg: transcriptional regulation in oocytes. Differentiation 73, 1–17.
Crossref | GoogleScholarGoogle Scholar | PubMed |

St Johnston, D. (1995). The intracellular localization of messenger RNAs. Cell 81, 161–170.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Stebbins-Boaz, B. , Hake, L. E. , and Richter, J. D. (1996). CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 15, 2582–2592.
PubMed |

Takizawa, P. A. , Sil, A. , Swedlow, J. R. , Herskowitz, I. , and Vale, R. D. (1997). Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389, 90–93.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Telford, N. A. , Watson, A. J. , and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Theurkauf, W. E. , Alberts, B. M. , Jan, Y. N. , and Jongens, T. A. (1993). A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169–1180.
PubMed |

Tong, Z. B. , and Nelson, L. M. (1999). A mouse gene encoding an oocyte antigen associated with autoimmune premature ovarian failure. Endocrinology 140, 3720–3726.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tong, Z. B. , Gold, L. , Pfeifer, K. E. , Dorward, H. , Lee, E. , Bondy, C. A. , Dean, J. , and Nelson, L. M. (2000). Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26, 267–268.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tremblay, K. , Vigneault, C. , McGraw, S. , and Sirard, M. A. (2005). Expression of cyclin B1 messenger RNA isoforms and initiation of cytoplasmic polyadenylation in the bovine oocyte. Biol. Reprod. 72, 1037–1044.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Uzbekova, S. , Roy-Sabau, M. , Dalbiès-Tran, R. , Perreau, C. , and Papillier, P. , et al. (2006). Zygote arrest 1 gene in pig, cattle and human: evidence of different transcript variants in male and female germ cells. Reprod. Biol. Endocrinol. 4, 12.
Crossref | GoogleScholarGoogle Scholar | PubMed |

van Eijk, M. J. , van Rooijen, M. A. , Modina, S. , Scesi, L. , and Folkers, G. , et al. (1999). Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol. Reprod. 60, 1093–1103.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vejlsted, M. , Avery, B. , Schmidt, M. , Greve, T. , Alexopoulos, N. , and Maddox-Hyttel, P. (2005). Ultrastructural and immunohistochemical characterization of the bovine epiblast. Biol. Reprod. 72, 678–686.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wickham, L. , Duchaine, T. , Luo, M. , Nabi, I. R. , and DesGroseillers, L. (1999). Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19, 2220–2230.
PubMed |

Wu, X. , Viveiros, M. M. , Eppig, J. J. , Bai, Y. , Fitzpatrick, S. L. , and Matzuk, M. M. (2003a). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–191.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wu, X. , Wang, P. , Brown, C. A. , Zilinski, C. A. , and Matzuk, M. M. (2003b). Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol. Reprod. 69, 861–867.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yoon, Y. J. , and Mowry, K. L. (2004). Xenopus Staufen is a component of a ribonucleoprotein complex containing Vg1 RNA and kinesin. Development 131, 3035–3045.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yu, J. , Deng, M. , Medvedev, S. , Yang, J. , Hecht, N. B. , and Schultz, R. M. (2004). Transgenic RNAi-mediated reduction of MSY2 in mouse oocytes results in reduced fertility. Dev. Biol. 268, 195–206.
Crossref | GoogleScholarGoogle Scholar | PubMed |