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      A Comparative Analysis of Oocyte Development in Mammals

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          Abstract

          Sexual reproduction requires the fertilization of a female gamete after it has undergone optimal development. Various aspects of oocyte development and many molecular actors in this process are shared among mammals, but phylogeny and experimental data reveal species specificities. In this chapter, we will present these common and distinctive features with a focus on three points: the shaping of the oocyte transcriptome from evolutionarily conserved and rapidly evolving genes, the control of folliculogenesis and ovulation rate by oocyte-secreted Growth and Differentiation Factor 9 and Bone Morphogenetic Protein 15, and the importance of lipid metabolism.

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          Human gene expression first occurs between the four- and eight-cell stages of preimplantation development.

          P Braude, V Bolton, S. Moore (1988)
          The earliest stages of development in most animals, including the few mammalian species that have been investigated, are regulated by maternally inherited information. Dependence on expression of the embryonic genome cannot be detected until the mid two-cell stage in the mouse, the four-cell stage in the pig (J. Osborn & C. Polge, personal communication), and the eight-cell stage in the sheep. Information about the timing of activation of the embryonic genome in the human is of relevance not only to the therapeutic practice of in vitro fertilization and embryo transfer (IVF), but more importantly for the successful development of techniques for the preimplantation diagnosis of certain inherited genetic diseases. We describe here changes in the pattern of polypeptides synthesized during the pre-implantation stages of human development, and demonstrate that some of the major qualitative changes which occur between the four- and eight-cell stages are dependent on transcription. In addition, it appears that cleavage is not sensitive to transcriptional inhibition until after the four-cell stage.
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            Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.

            Robert B. Gilchrist, Michelle Lane, Jeremy G B Thompson (2008)
            Oocyte quality is a key limiting factor in female fertility, yet we have a poor understanding of what constitutes oocyte quality or the mechanisms governing it. The ovarian follicular microenvironment and maternal signals, mediated primarily through granulosa cells (GCs) and cumulus cells (CCs), are responsible for nurturing oocyte growth, development and the gradual acquisition of oocyte developmental competence. However, oocyte-GC/CC communication is bidirectional with the oocyte secreting potent growth factors that act locally to direct the differentiation and function of CCs. Two important oocyte-secreted factors (OSFs) are growth-differentiation factor 9 and bone morphogenetic protein 15, which activate signaling pathways in CCs to regulate key genes and cellular processes required for CC differentiation and for CCs to maintain their distinctive phenotype. Hence, oocytes appear to tightly control their neighboring somatic cells, directing them to perform functions required for appropriate development of the oocyte. This oocyte-CC regulatory loop and the capacity of oocytes to regulate their own microenvironment by OSFs may constitute important components of oocyte quality. In support of this notion, it has recently been demonstrated that supplementing oocyte in vitro maturation (IVM) media with exogenous OSFs improves oocyte developmental potential, as evidenced by enhanced pre- and post-implantation embryo development. This new perspective on oocyte-CC interactions is improving our knowledge of the processes regulating oocyte quality, which is likely to have a number of applications, including improving the efficiency of clinical IVM and thereby providing new options for the treatment of infertility.
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              Growth differentiation factor-9 is required during early ovarian folliculogenesis.

              J. Dong, D Albertini, K Nishimori … (1996)
              Growth factors synthesized by ovarian somatic cells directly affect oocyte growth and function, but it is unclear whether oocyte-secreted factors play a reciprocal role in modulating somatic cell functions in vivo. During the functional analysis of members of the transforming growth factor-beta superfamily in mouse development, we have uncovered a new family member, growth differentiation factor-9 (GDF-9), which is required for ovarian folliculogenesis. GDF-9 messenger RNA is synthesized only in the oocyte from the primary one-layer follicle stage until after ovulation. Here we analyse ovaries from GDF-9-deficient female mice and demonstrate that primordial and primary one-layer follicles can be formed, but there is a block in follicular development beyond the primary one-layer follicle stage which leads to complete infertility. Oocyte growth and zona pellucida formation proceed normally, but other aspects of oocyte differentiation are compromised. Thus, GDF-9 is the first oocyte-derived growth factor required for somatic cell function in vivo.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Cells
                Journal ID (iso-abbrev): Cells
                Journal ID (publisher-id): cells
                Title: Cells
                Publisher: MDPI
                ISSN (Electronic): 2073-4409
                Publication date (Electronic): 17 April 2020
                Publication date Collection: April 2020
                Volume: 9
                Issue: 4
                Electronic Location Identifier: 1002
                Affiliations
                [1 ]INRAE, CNRS, Université de Tours, IFCE, PRC, F-37380 Nouzilly, France
                [2 ]CHU Bretonneau, Médecine et Biologie de la Reproduction-CECOS, 37044 Tours, France
                Author notes
                Author information
                https://orcid.org/0000-0002-0376-0641
                https://orcid.org/0000-0003-3653-8737
                Article
                Publisher ID: cells-09-01002
                DOI: 10.3390/cells9041002
                PMC ID: 7226043
                PubMed ID: 32316494
                SO-VID: 41b2fee6-2133-4150-bde4-3b571715a934
                Copyright © © 2020 by the authors.
                License:

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 14 February 2020
                Date accepted : 09 April 2020
                Categories
                Subject: Review

                Keywords: oocyte,mammals,evolution,gene expression,posttranscriptional control,gdf9,bmp15,lipids
                Data availability:
                Keywords: oocyte, mammals, evolution, gene expression, posttranscriptional control, gdf9, bmp15, lipids

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