Gene expression during the oocyte-to-embryo transition in mammals

The Jackson Laboratory, Bar Harbor, Maine 04609, USA.
Molecular Reproduction and Development (Impact Factor: 2.53). 09/2009; 76(9):805-18. DOI: 10.1002/mrd.21038
Source: PubMed


The seminal question in modern developmental biology is the origins of new life arising from the unification of sperm and egg. The roots of this question begin from 19th to 20th century embryologists studying fertilization and embryogenesis. Although the revolution of molecular biology has yielded significant insight into the complexity of this process, the overall orchestration of genes, molecules, and cells is still not fully formed. Early mammalian development, specifically the oocyte-to-embryo transition, is essentially under "maternal command" from factors deposited in the cytoplasm during oocyte growth, independent of de novo transcription from the nascent embryo. Many of the advances in understanding this developmental period occurred in tandem with application of new methods and techniques from molecular biology, from protein electrophoresis to sequencing and assemblies of whole genomes. From this bed of knowledge, it appears that precise control of mRNA translation is a key regulator coordinating the molecular and cellular events occurring during oocyte-to-embryo transition. Notably, oocyte transcriptomes share, yet retain some uniqueness, common genetic motifs among all chordates. The common genetic motifs typically define fundamental processes critical for cellular maintenance, whereas the unique genetic features may be a source of variation and a substrate for sexual selection, genetic drift, or gene flow. One purpose for this complex interplay among genes, proteins, and cells may allow for evolution to transform and act upon the underlying processes, at molecular, structural and organismal levels, to increase diversity, which is the ultimate goal of sexual reproduction.

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    • "After fertilization, erasure of the oogenic program and reprogramming by establishing the embryonic program into totipotent zygotes are coordinately regulated (Pellettieri et al., 2003; DeRenzo and Seydoux, 2004; Stitzel and Seydoux, 2007). This process is called maternal-to-zygotic transition (MZT) and is accompanied by degradation of maternal mRNAs and proteins and transcription of zygotic genes (Keshet et al., 1988; Evsikov and Marín de Evsikova, 2009; Shin et al., 2010). Oocyte-derived mRNAs are degraded shortly after fertilization, and ∼90% of RNAs stored in the oocyte are degraded by the 2-cell stage, which is an essential process for embryogenesis (Stitzel and Seydoux, 2007). "
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    ABSTRACT: During the maternal-to-zygotic transition (MZT), maternal proteins in oocytes are degraded by the ubiquitin-proteasome system (UPS), and new proteins are synthesized from the zygotic genome. However, the specific mechanisms underlying the UPS at the MZT are not well understood. We identified a molecule named zygote-specific proteasome assembly chaperone (ZPAC) that is specifically expressed in mouse gonads, and expression of ZPAC was transiently increased at the mouse MZT. ZPAC formed a complex with Ump1 and associated with precursor forms of 20S proteasomes. Transcription of ZPAC genes was also under the control of an autoregulatory feedback mechanism for the compensation of reduced proteasome activity similar to Ump1 and 20S proteasome subunit gene expression. Knockdown of ZPAC in early embryos caused a significant reduction of proteasome activity and decrease in Ump1 and mature proteasomes, leading to accumulation of proteins that need to be degraded at the MZT and early developmental arrest. Therefore, a unique proteasome assembly pathway mediated by ZPAC is important for progression of the mouse MZT.
    Biology Open 02/2013; 2(2):170-82. DOI:10.1242/bio.20123020 · 2.42 Impact Factor
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    • "The ability of the oocyte to acquire developmental competence and to support early embryonic development is the result of the regulation of its transcriptional activity and the synergic actions of gonadotropins and growth factors (Menezo and Elder 2011). Regulation of transcriptional activity includes timely translation of stored maternal transcripts, post-translational modification of stored or newly synthesized proteins (this sets the exact timing for cellular events), and processes involved in degradation of proteins and mRNAs (Song and Wessel 2005; Stitzel and Seydoux 2007; Evsikov and Marin de 2009). All of these are influenced by hormones, genetic, nutritional, immunological factors and age, as well as environmental impacts (Grøndahl et al. 2010). "
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    ABSTRACT: A recently emerged concept utilizing a controlled environmental impact as a treatment for cells and tissues aims to improve neither the in vitro conditions nor the procedures, but the cell itself. Hydrostatic pressure stress emerged as the most controllable and most effective stressor, proving the principle that controlled stress improves cell performance in in vitro procedures, whereas further studies using different stressors (osmotic, oxidative or mechanic stresses) supported the principle. The present summary reviews studies of various stress treatments to treat oocytes of three species (murine, porcine, human) before vitrification, in vitro maturation, enucleation and somatic cell nuclear transfer. Eventually, cleavage and blastocyst rates and--in cases when hydrostatic pressure was used--blastocyst cell number and birth rates as well were significantly improved compared to untreated controls.
    Reproduction in Domestic Animals 08/2012; 47 Suppl 4(s4):197-206. DOI:10.1111/j.1439-0531.2012.02076.x · 1.52 Impact Factor
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    • "Developmental exposure of male germ cells to 5 - azacytidine results in abnormal preimplantation devel - opment in rats . Biol . Reprod . 55 , 1155 – 1162 . Evsikov , A . V . , and Marin de Evsikova , C . ( 2009 ) . Gene expression during the oocyte - to - embryo transition in mammals . Mol . Reprod . Dev . 76 , 805 – 818 ."
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    ABSTRACT: Embryonic development is a complex and dynamic process with frequent changes in gene expression, ultimately leading to cellular differentiation and commitment of various cell lines. These changes are likely preceded by changes to signaling cascades and/or alterations to the epigenetic program in specific cells. The process of epigenetic remodeling begins early in development. In fact, soon after the union of sperm and egg massive epigenetic changes occur across the paternal and maternal epigenetic landscape. The epigenome of these cells includes modifications to the DNA itself, in the form of DNA methylation, as well as nuclear protein content and modification, such as modifications to histones. Sperm chromatin is predominantly packaged by protamines, but following fertilization the sperm pronucleus undergoes remodeling in which maternally derived histones replace protamines, resulting in the relaxation of chromatin and ultimately decondensation of the paternal pronucleus. In addition, active DNA demethylation occurs across the paternal genome prior to the first cell division, effectively erasing many spermatogenesis derived methylation marks. This complex interplay begins the dynamic process by which two haploid cells unite to form a diploid organism. The biology of these events is central to the understanding of sexual reproduction, yet our knowledge regarding the mechanisms involved is extremely limited. This review will explore what is known regarding the post-fertilization epigenetic alterations of the paternal chromatin and the implications suggested by the available literature.
    Frontiers in Genetics 07/2012; 3:143. DOI:10.3389/fgene.2012.00143
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